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Engineered Meganucleases for Genome Engineering Purposes

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Site-directed insertion of transgenes

Part of the book series: Topics in Current Genetics ((TCG,volume 23))

Abstract

Over the past 15 years, site-directed genome modification has proven to be an efficient and robust approach. Meganucleases, sequence-specific endonucleases with long recognition sites, represent one of several tools described in this book that can be used for this purpose. This chapter will review the early stages of the technology (with the first strand break-induced gene targeting with I-SceI), and describe the recent advances in protein engineering that have led to the making of tailored meganucleases. We will then summarize the data and strategies available today regarding their use for site-directed genome modification. In the last section, we will discuss the latest data available on Transcription activator like effectors proteins as they have recently emerged as a promising new tool for genome modifications.

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References

  • Alwin S, Gere MB, Guhl E, Effertz K, Barbas CF 3rd, Segal DJ, Weitzman MD, Cathomen T (2005) Custom zinc-finger nucleases for use in human cells. Mol Ther 12:610–617

    Article  CAS  Google Scholar 

  • Argast GM, Stephens KM, Emond MJ, Monnat RJ Jr (1998) I-PpoI and I-CreI homing site sequence degeneracy determined by random mutagenesis and sequential in vitro enrichment. J Mol Biol 280:345–353

    Article  CAS  Google Scholar 

  • Arimondo PB, Thomas CJ, Oussedik K, Baldeyrou B, Mahieu C, Halby L, Guianvarc’h D, Lansiaux A, Hecht SM, Bailly C, Giovannangeli C (2006) Exploring the cellular activity of camptothecin-triple-helix-forming oligonucleotide conjugates. Mol Cell Biol 26:324–333

    Article  CAS  Google Scholar 

  • Arnould S, Chames P, Perez C, Lacroix E, Duclert A, Epinat JC, Stricher F, Petit AS, Patin A, Guillier S, Rolland S, Prieto J, Blanco FJ, Bravo J, Montoya G, Serrano L, Duchateau P, Paques F (2006) Engineering of large numbers of highly specific homing endonucleases that induce recombination on novel DNA targets. J Mol Biol 355:443–458

    Article  CAS  Google Scholar 

  • Arnould S, Perez C, Cabaniols JP, Smith J, Gouble A, Grizot S, Epinat JC, Duclert A, Duchateau P, Paques F (2007) Engineered I-CreI derivatives cleaving sequences from the human XPC gene can induce highly efficient gene correction in mammalian cells. J Mol Biol 371:49–65

    Article  CAS  Google Scholar 

  • Arnould S, Delenda C, Grizot S, Desseaux C, Paques F, Silva GH, Smith J (2011) The I-CreI meganuclease and its engineered derivatives: applications from cell modification to gene therapy. Protein Eng Des Sel PEDS 24:27–31

    Article  CAS  Google Scholar 

  • Ashworth J, Havranek JJ, Duarte CM, Sussman D, Monnat RJ Jr, Stoddard BL, Baker D (2006) Computational redesign of endonuclease DNA binding and cleavage specificity. Nature 441:656–659

    Article  CAS  Google Scholar 

  • Ashworth J, Taylor GK, Havranek JJ, Quadri SA, Stoddard BL, Baker D (2010) Computational reprogramming of homing endonuclease specificity at multiple adjacent base pairs. Nucleic Acids Res 38:5601–5608

    Article  CAS  Google Scholar 

  • Aten JA, Stap J, Krawczyk PM, Van Oven CH, Hoebe RA, Essers J, Kanaar R (2004) Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303:92–95

    Article  CAS  Google Scholar 

  • Aubert M, Ryu BY, Banks L, Rawlings DJ, Scharenberg AM, Jerome KR (2011) Successful targeting and disruption of an integrated reporter lentivirus using the engineered homing endonuclease Y2 I-AniI. PLoS One 6:e16825

    Article  CAS  Google Scholar 

  • Belfort M (2003) Two for the price of one: a bifunctional intron-encoded DNA endonuclease-RNA maturase. Genes Dev 17:2860–2863

    Article  CAS  Google Scholar 

  • Belfort M, Derbyshire V, Parker MM, Cousineau B, Lambowitz AM (2002) Mobile introns: pathways and proteins. In: Craig N, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II. ASM Press, Washington, DC, pp 761–783

    Google Scholar 

  • Bezzubova O, Silbergleit A, Yamaguchi-Iwai Y, Takeda S, Buerstedde JM (1997) Reduced X-ray resistance and homologous recombination frequencies in a RAD54/ mutant of the chicken DT40 cell line. Cell 89:185–193

    Article  CAS  Google Scholar 

  • Blundell PA, Rudenko G, Borst P (1996) Targeting of exogenous DNA into Trypanosoma brucei requires a high degree of homology between donor and target DNA. Mol Biochem Parasitol 76:215–229

    Article  CAS  Google Scholar 

  • Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436

    Article  CAS  Google Scholar 

  • Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326:1509–1512

    Article  CAS  Google Scholar 

  • Bogdanove AJ, Schornack S, Lahaye T (2010) TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 13:394–401

    Article  CAS  Google Scholar 

  • Bolduc JM, Spiegel PC, Chatterjee P, Brady KL, Downing ME, Caprara MG, Waring RB, Stoddard BL (2003) Structural and biochemical analyses of DNA and RNA binding by a bifunctional homing endonuclease and group I intron splicing factor. Genes Dev 17:2875–2888

    Article  CAS  Google Scholar 

  • Bonas U, Stall RE, Staskawicz B (1989) Genetic and structural characterization of the avirulence gene avrBs3 from Xanthomonas campestris pv. vesicatoria. Mol Gen Genet 218:127–136

    Article  CAS  Google Scholar 

  • Bronson SK, Smithies O (1994) Altering mice by homologous recombination using embryonic stem cells. J Biol Chem 269:27155–27158

    CAS  Google Scholar 

  • Buerstedde JM, Takeda S (1991) Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell 67:179–188

    Article  CAS  Google Scholar 

  • Cabaniols JP, Paques F (2008) Robust cell line development using meganucleases. Methods Mol Biol 435:31–45

    Article  CAS  Google Scholar 

  • Cabaniols JP, Mathis L, Delenda C (2009) Targeted gene modifications in drug discovery and development. Curr Opin Pharmacol 9:657–663

    Article  CAS  Google Scholar 

  • Cabaniols JP, Ouvry C, Lamamy V, Fery I, Craplet ML, Moulharat N, Guenin SP, Bedut S, Nosjean O, Ferry G, Devavry S, Jacqmarcq C, Lebuhotel C, Mathis L, Delenda C, Boutin JA, Duchateau P, Coge F, Paques F (2010) Meganuclease-driven targeted integration in CHO-K1 cells for the fast generation of HTS-compatible cell-based assays. J Biomol Screen 15:956–967

    Article  CAS  Google Scholar 

  • Cavalier-Smith T (1985) Selfish DNA and the origin of introns. Nature 315(6017):283–284

    Article  CAS  Google Scholar 

  • Capecchi MR (2) Generating mice with targeted mutations. Nat Med 7:1086–1090

    Article  CAS  Google Scholar 

  • Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39(12):e82

    Article  CAS  Google Scholar 

  • Chames P, Epinat JC, Guillier S, Patin A, Lacroix E, Paques F (2005) In vivo selection of engineered homing endonucleases using double-strand break induced homologous recombination. Nucleic Acids Res 33:e178

    Article  CAS  Google Scholar 

  • Chen Z, Wen F, Sun N, Zhao H (2009) Directed evolution of homing endonuclease I-SceI with altered sequence specificity gzp [pii] 10.1093/protein/gzp. Protein Eng Des Sel PEDS 22:249–256

    Article  CAS  Google Scholar 

  • Chevalier BS, Stoddard BL (2) Homing endonucleases: structural and functional insight into the catalysis of intron/intein mobility. Nucleic Acids Res 29:3757–3774

    Article  Google Scholar 

  • Chevalier BS, Monnat RJ Jr, Stoddard BL (2) The homing endonuclease I-CreI uses three metals, one of which is shared between the two active sites. Nat Struct Biol 8:312–316

    Article  CAS  Google Scholar 

  • Chevalier BS, Kortemme T, Chadsey MS, Baker D, Monnat RJ, Stoddard BL (2002) Design, activity, and structure of a highly specific artificial endonuclease. Mol Cell 10:895–905

    Article  CAS  Google Scholar 

  • Chevalier B, Turmel M, Lemieux C, Monnat RJ Jr, Stoddard BL (2003) Flexible DNA target site recognition by divergent homing endonuclease isoschizomers I-CreI and I-MsoI. J Mol Biol 329:253–269

    Article  CAS  Google Scholar 

  • Chiurazzi M, Ray A, Viret JF, Perera R, Wang XH, Lloyd AM, Signer ER (1996) Enhancement of somatic intrachromosomal homologous recombination in Arabidopsis by the HO endonuclease. Plant Cell 8:2057–2066

    CAS  Google Scholar 

  • Choulika A, Perrin A, Dujon B, 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

    CAS  Google Scholar 

  • Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761

    Article  CAS  Google Scholar 

  • Cohen-Tannoudji M, Robine S, Choulika A, Pinto D, El Marjou F, Babinet C, Louvard D, Jaisser F (1998) I-SceI-induced gene replacement at a natural locus in embryonic stem cells. Mol Cell Biol 18:1444–1448

    CAS  Google Scholar 

  • Colleaux L, D’auriol L, Galibert F, Dujon B (1988) Recognition and cleavage site of the intron-encoded omega transposase. Proc Natl Acad Sci U S A 85:6022–6026

    Article  CAS  Google Scholar 

  • Colleaux L, Rougeulle C, Avner P, Dujon B (1993) Rapid physical mapping of YAC inserts by random integration of I-Sce I sites. Hum Mol Genet 2:265–271

    Article  CAS  Google Scholar 

  • Cost GJ, Freyvert Y, Vafiadis A, Santiago Y, Miller JC, Rebar E, Collingwood TN, Snowden A, Gregory PD (2010) BAK and BAX deletion using zinc-finger nucleases yields apoptosis-resistant CHO cells. Biotechnol Bioeng 105:330–340

    Article  CAS  Google Scholar 

  • Cox MM, Layton SL, Jiang T, Cole K, Hargis BM, Berghman LR, Bottje WG, Kwon YM (2007) Scarless and site-directed mutagenesis in Salmonella enteritidis chromosome. BMC Biotechnol 7:59

    Article  CAS  Google Scholar 

  • Cradick TJ, Keck K, Bradshaw S, Jamieson AC, Mccaffrey AP (2010) Zinc-finger nucleases as a novel therapeutic strategy for targeting hepatitis B virus DNAs. Mol Ther 18:947–954

    Article  CAS  Google Scholar 

  • Daboussi F, Zaslavskiy M, Poirot L, Loperfido M, Gouble A, Guyot V, Leduc S, Galetto R, Grizot S, Oficjalska D, Perez C, Delacote F, Dupuy A, Chion-Sotinel I, Le Clerre D, Lebuhotel C, Danos O, Lemaire F, Oussedik K, Cedrone F, Epinat JC, Smith J, Dickson G, Popplewell L, Koo T, Vandendriessche T, Chuah MK, Duclert A, Duchateau P, Paques F (2012) Chromosomal context and epigenetic mechanisms control the efficacy of genome editing by rare-cutting designer endonucleases. Nucleic Acids Res. Epub Mar 29

    Google Scholar 

  • Doetschman T, Gregg RG, Maeda N, Hooper ML, Melton DW, Thompson S, Smithies O (1987) Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature 330:576–578

    Article  CAS  Google Scholar 

  • Donoho G, Jasin M, 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

    CAS  Google Scholar 

  • Doyon JB, Pattanayak V, Meyer CB, Liu DR (2006) Directed evolution and substrate specificity profile of homing endonuclease I-SceI. J Am Chem Soc 128:2477–2484

    Article  CAS  Google Scholar 

  • Doyon Y, Mccammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, Amora R, Hocking TD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Amacher SL (2008) Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol 26:702–708

    Article  CAS  Google Scholar 

  • Duan X, Gimble FS, Quiocho FA (1997) Crystal structure of PI-SceI, a homing endonuclease with protein splicing activity. Cell 89:555–564

    Article  CAS  Google Scholar 

  • Eisenschmidt K, Lanio T, Simoncsits A, Jeltsch A, Pingoud V, Wende W, Pingoud A (2005) Developing a programmed restriction endonuclease for highly specific DNA cleavage. Nucleic Acids Res 33:7039–7047

    Article  CAS  Google Scholar 

  • Elliott B, Richardson C, Winderbaum J, Nickoloff JA, Jasin M (1998) Gene conversion tracts from double-strand break repair in mammalian cells. Mol Cell Biol 18:93–101

    CAS  Google Scholar 

  • Engler C, Kandzia R, Marillonnet S (2008) A one pot, one step, precision cloning method with high throughput capability. PLoS One 3:e3647

    Article  CAS  Google Scholar 

  • Epinat JC, Arnould S, Chames P, Rochaix P, Desfontaines D, Puzin C, Patin A, Zanghellini A, Paques F, Lacroix E (2003) A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells. Nucleic Acids Res 31:2952–2962

    Article  CAS  Google Scholar 

  • Fajardo-Sanchez E, Stricher F, Paques F, Isalan M, Serrano L (2008) Computer design of obligate heterodimer meganucleases allows efficient cutting of custom DNA sequences Nucleic Acids Res 36:2163–2173

    CAS  Google Scholar 

  • Flannagan RS, Linn T, Valvano MA (2008) A system for the construction of targeted unmarked gene deletions in the genus Burkholderia. Environ Microbiol 10:1652–1660

    Article  CAS  Google Scholar 

  • Flick KE, Jurica MS, Monnat RJ Jr, Stoddard BL (1998) DNA binding and cleavage by the nuclear intron-encoded homing endonuclease I-PpoI. Nature 394:96–101

    Article  CAS  Google Scholar 

  • Flisikowska T, Thorey IS, Offner S, Ros F, Lifke V, Zeitler B, Rottmann O, Vincent A, Zhang L, Jenkins S, Niersbach H, Kind AJ, Gregory PD, Schnieke AE, Platzer J (2011) Efficient immunoglobulin gene disruption and targeted replacement in rabbit using zinc finger nucleases. PLoS One 6:e21045

    Article  CAS  Google Scholar 

  • Friedhoff P, Franke I, Meiss G, Wende W, Krause KL, Pingoud A (1999) A similar active site for non-specific and specific endonucleases. Nat Struct Biol 6:112–113

    Article  CAS  Google Scholar 

  • Galetto R, Duchateau P, Paques F (2009) Targeted approaches for gene therapy and the emergence of engineered meganucleases. Expert Opin Biol Ther 9:1289–1303

    Article  CAS  Google Scholar 

  • Gao H, Smith J, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, Jantz D, Lyznik LA (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J 61:176–187

    Article  CAS  Google Scholar 

  • Geissler R, Scholze H, Hahn S, Streubel J, Bonas U, Behrens SE, Boch J (2011) Transcriptionnal Activators of Human genes with progammable DNA-specificity. PLoS ONE 6:e19509

    Article  CAS  Google Scholar 

  • Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, Wood A, Cui X, Meng X, Vincent A, Lam S, Michalkiewicz M, Schilling R, Foeckler J, Kalloway S, Weiler H, Menoret S, Anegon I, Davis GD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jacob HJ, Buelow R (2009) Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325:433

    Article  CAS  Google Scholar 

  • Gimble FS (2000) Invasion of a multitude of genetic niches by mobile endonuclease genes. FEMS Microbiol Lett 185:99–107

    Article  CAS  Google Scholar 

  • Gimble FS, Moure CM, Posey KL (2003) Assessing the plasticity of DNA target site recognition of the PI-SceI homing endonuclease using a bacterial two-hybrid selection system. J Mol Biol 334:993–1008

    Article  CAS  Google Scholar 

  • Glover L, Mcculloch R, Horn D (2008) Sequence homology and microhomology dominate chromosomal double-strand break repair in African trypanosomes. Nucleic Acids Res 36:2608–2618

    Article  CAS  Google Scholar 

  • Gouble A, Smith J, Bruneau S, Perez C, Guyot V, Cabaniols JP, Leduc S, Fiette L, Ave P, Micheau B, Duchateau P, Paques F (2006) Efficient in toto targeted recombination in mouse liver by meganuclease-induced double-strand break. J Gene Med 8:616–622

    Article  CAS  Google Scholar 

  • Grabher C, Wittbrodt J (2008) Recent advances in meganuclease-and transposon-mediated transgenesis of medaka and zebrafish. Methods Mol Biol 461:521–539

    Article  CAS  Google Scholar 

  • Grizot S, Smith J, Daboussi F, Prieto J, Redondo P, Merino N, Villate M, Thomas S, Lemaire L, Montoya G, Blanco FJ, Paques F, Duchateau P (2009) Efficient targeting of a SCID gene by an engineered single-chain homing endonuclease. Nucleic Acids Res 37:5405–5419

    Article  CAS  Google Scholar 

  • Grizot S, Epinat JC, Thomas S, Duclert A, Rolland S, Paques F, Duchateau P (2010) Generation of redesigned homing endonucleases comprising DNA-binding domains derived from two different scaffolds. Nucleic Acids Res 38:2006–2018

    Article  CAS  Google Scholar 

  • Grizot S, Duclert A, Thomas S, Duchateau P, Paques F (2011) Context dependence between subdomains in the DNA binding interface of the I-CreI homing endonuclease. Nucleic Acids Res 39:6124–6136

    Article  CAS  Google Scholar 

  • Grosse S, Huot N, Mahiet C, Arnould S, Barradeau S, Clerre DL, Chion-Sotinel I, Jacqmarcq C, Chapellier B, Ergani A, Desseaux C, Cedrone F, Conseiller E, Paques F, Labetoulle M, Smith J (2011) Meganuclease-mediated inhibition of HSV1 infection in cultured cells. Mol Ther 19:694–702

    Article  CAS  Google Scholar 

  • Gurlebeck D, Szurek B, Bonas U (2005) Dimerization of the bacterial effector protein AvrBs3 in the plant cell cytoplasm prior to nuclear import. Plant J 42:175–187

    Article  CAS  Google Scholar 

  • Hauschild J, Petersen B, Santiago Y, Queisser AL, Carnwath JW, Lucas-Hahn A, Zhang L, Meng X, Gregory PD, Schwinzer R, Cost GJ, Niemann H (2011) Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc Natl Acad Sci U S A 108:12013–12017

    Article  CAS  Google Scholar 

  • Hauschild J, Petersen B, Santiago Y, Queisser AL, Carnwath JW, Lucas-Hahn A, Zhang L, Meng X, Gregory PD, Schwinzer R, Cost GJ, Niemann H (2011) Proc Natl Acad Sci USA 108:12013–12017

    Article  CAS  Google Scholar 

  • Heath PJ, Stephens KM, Monnat RJ Jr, Stoddard BL (1997) The structure of I-Crel, a group I intron-encoded homing endonuclease. Nat Struct Biol 4:468–476

    Article  CAS  Google Scholar 

  • Hinnen A, Hicks JB, Fink GR (1978) Transformation of yeast. Proc Natl Acad Sci U S A 75:1929–1933

    Article  CAS  Google Scholar 

  • Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, Dekelver RC, Katibah GE, Amora R, Boydston EA, Zeitler B, Meng X, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R (2009) Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol 27:851–857

    Article  CAS  Google Scholar 

  • Hockemeyer DWH, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, Zeitler B, Cherone JM, Meng X, Hinkley SJ, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R (2011) Genetic engineering of human pluripotent cells using TALE nucleases. Nature Biotechnol 29:731–734

    Article  CAS  Google Scholar 

  • Horzempa J, Shanks RM, Brown MJ, Russo BC, O’Dee DM, Nau GJ (2010) Utilization of an unstable plasmid and the I-SceI endonuclease to generate routine markerless deletion mutants in Francisella tularensis. J Microbiol Methods 80:106–108

    Article  CAS  Google Scholar 

  • Huang P, Xiao A, Zhou M, Zhu Z, Lin S, Zhang B (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29:699–700

    Article  CAS  Google Scholar 

  • Jacquier A, Dujon B (1985) An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 41:383–394

    Article  CAS  Google Scholar 

  • Jarjour J, West-Foyle H, Certo MT, Hubert CG, Doyle L, Getz MM, Stoddard BL, Scharenberg AM (2009) High-resolution profiling of homing endonuclease binding and catalytic specificity using yeast surface display. Nucleic Acids Res 37:6871–6880

    Article  CAS  Google Scholar 

  • Jurica MS, Monnat RJ Jr, Stoddard BL (1998) DNA recognition and cleavage by the LAGLIDADG homing endonuclease I-CreI. Mol Cell 2:469–476

    Article  CAS  Google Scholar 

  • Koller BH, Smithies O (1989) Inactivating the beta 2-microglobulin locus in mouse embryonic stem cells by homologous recombination. Proc Natl Acad Sci U S A 86:8932–8935

    Article  CAS  Google Scholar 

  • Kostriken R, Strathern JN, Klar AJ, Hicks JB, Heffron F (1983) A site-specific endonuclease essential for mating-type switching in Saccharomyces cerevisiae. Cell 35:167–174

    Article  CAS  Google Scholar 

  • Kuhlmann UC, Moore GR, James R, Kleanthous C, Hemmings AM (1999) Structural parsimony in endonuclease active sites: should the number of homing endonuclease families be redefined? FEBS Lett 463:1–2

    Article  CAS  Google Scholar 

  • Lambowitz AM, Caprara MG, Zimmerly S, Perlman PS (1999) Group I and group II ribozymes as RNPs: clues to the past and guides to the future. In: The RNA world, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Li H, Pellenz S, Ulge U, Stoddard BL, Monnat RJ Jr (2009) Generation of single-chain LAGLIDADG homing endonucleases from native homodimeric precursor proteins. Nucleic Acids Res 37:1650–1662

    Article  CAS  Google Scholar 

  • Li T, Huang S, Jiang WZ, Wright D, Spalding MH, Weeks DP, Yang B (2011) TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 39:359–372

    Article  CAS  Google Scholar 

  • Li T, Huang S, Zhao X, Wright DA, Carpenter S, Spalding MH, Weeks DP, Yang B (2011) Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 39(14):6315–6325

    Article  CAS  Google Scholar 

  • Liang F, Han M, Romanienko PJ, Jasin M (1998) Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci U S A 95:5172–5177

    Article  CAS  Google Scholar 

  • Liu PQ, Chan EM, Cost GJ, Zhang L, Wang J, Miller JC, Guschin DY, Reik A, Holmes MC, Mott JE, Collingwood TN, Gregory PD (2010) Generation of a triple-gene knockout mammalian cell line using engineered zinc-finger nucleases. Biotechnol Bioeng 106:97–105

    CAS  Google Scholar 

  • Loeber J, Pan FC, Pieler T (2009) Generation of transgenic frogs. Methods Mol Biol 561:65–72

    Article  CAS  Google Scholar 

  • Loizos N, Silva GH, Belfort M (1996) Intron-encoded endonuclease I-TevII binds across the minor groove and induces two distinct conformational changes in its DNA substrate. J Mol Biol 255:412–424

    Article  CAS  Google Scholar 

  • Lombardo A, Genovese P, Beausejour CM, Colleoni S, Lee YL, Kim KA, Ando D, Urnov FD, Galli C, Gregory PD, Holmes MC, Naldini L (2007) Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 25:1298–1306

    Article  CAS  Google Scholar 

  • Lucas P, Otis C, Mercier JP, Turmel M, Lemieux C (2) Rapid evolution of the DNA-binding site in LAGLIDADG homing endonucleases. Nucleic Acids Res 29:960–969

    Article  Google Scholar 

  • Maeder ML, Thibodeau-Beganny S, Osiak A, Wright DA, Anthony RM, Eichtinger M, Jiang T, Foley JE, Winfrey RJ, Townsend JA, Unger-Wallace E, Sander JD, Muller-Lerch F, Fu F, Pearlberg J, Gobel C, Dassie JP, Pruett-Miller SM, Porteus MH, Sgroi DC, Iafrate AJ, Dobbs D, Mccray PB Jr, Cathomen T, Voytas DF, Joung JK (2008) Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell 31:294–301

    Article  CAS  Google Scholar 

  • Maggert KA, Gong WJ, Golic KG (2008) Methods for homologous recombination in Drosophila. Methods Mol Biol 420:155–174

    Article  CAS  Google Scholar 

  • Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu JK (2011) De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci U S A 108:2623–2628

    Article  CAS  Google Scholar 

  • Majumdar A, Muniandy PA, Liu J, Liu JL, Liu ST, Cuenoud B, Seidman MM (2008) Targeted gene knock in and sequence modulation mediated by a psoralen-linked triplex-forming oligonucleotide. J Biol Chem 283:11244–11252

    Article  CAS  Google Scholar 

  • Mansour SL, Thomas KR, Capecchi MR (1988) Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature 336:348–352

    Article  CAS  Google Scholar 

  • Marcaida MJ, Prieto J, Redondo P, Nadra AD, Alibes A, Serrano L, Grizot S, Duchateau P, Paques F, Blanco FJ, Montoya G (2008) Crystal structure of I-DmoI in complex with its target DNA provides new insights into meganuclease engineering. Proc Natl Acad Sci U S A 105:16888–16893

    Article  CAS  Google Scholar 

  • Marcaida MJ, Munoz IG, Blanco FJ, Prieto J, Montoya G (2010) Homing endonucleases: from basics to therapeutic applications. Cell Mol Life Sci 67:727–748

    Article  CAS  Google Scholar 

  • Mashimo T, Takizawa A, Voigt B, Yoshimi K, Hiai H, Kuramoto T, Serikawa T (2010) Generation of knockout rats with X-linked severe combined immunodeficiency (X-SCID) using zinc-finger nucleases. PLoS One 5:e8870

    Article  CAS  Google Scholar 

  • Mcconnell Smith A, Takeuchi R, Pellenz S, Davis L, Maizels N, Monnat RJ Jr, Stoddard BL (2009) Generation of a nicking enzyme that stimulates site-specific gene conversion from the I-AniI LAGLIDADG homing endonuclease. Proc Natl Acad Sci U S A 106:5099–5104

    Article  CAS  Google Scholar 

  • Meng X, Noyes MB, Zhu LJ, Lawson ND, Wolfe SA (2008) Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol 26:695–701

    Article  CAS  Google Scholar 

  • Metzger MJ, Mcconnell-Smith A, Stoddard BL, Miller AD (2011) Single-strand nicks induce homologous recombination with less toxicity than double-strand breaks using an AAV vector template. Nucleic Acids Res 39:926–935

    Article  CAS  Google Scholar 

  • Miller DG, Petek LM, Russell DW (2003) Human gene targeting by adeno-associated virus vectors is enhanced by DNA double-strand breaks. Mol Cell Biol 23:3550–3557

    Article  CAS  Google Scholar 

  • Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, Dulay GP, Hua KL, Ankoudinova I, Cost GJ, Urnov FD, Zhang HS, Holmes MC, Zhang L, Gregory PD, Rebar EJ (2010) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29:143–148

    Article  CAS  Google Scholar 

  • Morbitzer R, Elsaesser J, Hausner J, Lahaye T (2011) Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res 39(13):5790–5799

    Article  CAS  Google Scholar 

  • Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326:1501

    Article  CAS  Google Scholar 

  • Moure CM, Gimble FS, Quiocho FA (2002) Crystal structure of the intein homing endonuclease PI-SceI bound to its recognition sequence. Nat Struct Biol 9:764–770

    Article  CAS  Google Scholar 

  • Moure CM, Gimble FS, Quiocho FA (2003) The crystal structure of the gene targeting homing endonuclease I-SceI reveals the origins of its target site specificity. J Mol Biol 334:685–695

    Article  CAS  Google Scholar 

  • Moynahan ME, Jasin M (1997) Loss of heterozygosity induced by a chromosomal double-strand break. Proc Natl Acad Sci U S A 94:8988–8993

    Article  CAS  Google Scholar 

  • Munoz IG, Prieto J, Subramanian S, Coloma J, Redondo P, Villate M, Merino N, Marenchino M, D’Abramo M, Gervasio FL, Grizot S, Daboussi F, Smith J, Chion-Sotinel I, Paques F, Duchateau P, Alibes A, Stricher F, Serrano L, Blanco FJ, Montoya G (2011) Molecular basis of engineered meganuclease targeting of the endogenous human RAG1 locus. Nucleic Acids Res 39:729–743

    Article  CAS  Google Scholar 

  • Murphy KC (1998) Use of bacteriophage lambda recombination functions to promote gene replacement in Escherichia coli. J Bacteriol 180:2063–2071

    CAS  Google Scholar 

  • Mussolino C, Morbitzer R, Lutge F, Dannemann N, Lahaye T, Cathomen T (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39:9283–9293

    Article  CAS  Google Scholar 

  • Nickoloff JA, Chen EY, Heffron F (1986) A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc Natl Acad Sci U S A 83:7831–7835

    Article  CAS  Google Scholar 

  • Niu Y, Tenney K, Li H, Gimble FS (2008) Engineering variants of the I-SceI homing endonuclease with strand-specific and site-specific DNA-nicking activity. J Mol Biol 382:188–202

    Article  CAS  Google Scholar 

  • Nolan T, Papathanos P, Windbichler N, Magnusson K, Benton J, Catteruccia F, Crisanti A (2011) Developing transgenic anopheles mosquitoes for the sterile insect technique. Genetica 139:33–39

    Article  CAS  Google Scholar 

  • Ochiai H, Sakamoto N, Suzuki K, Akasaka K, Yamamoto T (2008) The Ars insulator facilitates I-SceI meganuclease-mediated transgenesis in the sea urchin embryo. Dev Dyn 237:2475–2482

    Article  CAS  Google Scholar 

  • Ogino H, Mcconnell WB, Grainger RM (2006) Highly efficient transgenesis in Xenopus tropicalis using I-SceI meganuclease. Mech Dev 123:103–113

    Article  CAS  Google Scholar 

  • Ogino H, Mcconnell WB, Grainger RM (2006) High-throughput transgenesis in Xenopus using I-SceI meganuclease. Nat Protoc 1:1703–1710

    Article  CAS  Google Scholar 

  • Orr-Weaver TL, Szostak JW, Rothstein RJ (1981) Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A 78:6354–6358

    Article  CAS  Google Scholar 

  • Orr-Weaver TL, Szostak JW, Rothstein RJ (1983) Genetic applications of yeast transformation with linear and gapped plasmids. Methods Enzymol 101:228–245

    Article  CAS  Google Scholar 

  • Pan FC, Chen Y, Loeber J, Henningfeld K, Pieler T (2006) I-SceI meganuclease-mediated transgenesis in Xenopus. Dev Dyn 235:247–252

    Article  CAS  Google Scholar 

  • Paques F, Duchateau P (2007) Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr Gen Ther 7:49–66

    Article  CAS  Google Scholar 

  • Paques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63:349–404

    CAS  Google Scholar 

  • Perez C, Guyot V, Cabaniols JP, Gouble A, Micheaux B, Smith J, Leduc S, Paques F, Duchateau P (2005) Factors affecting double-strand break-induced homologous recombination in mammalian cells. Biotechniques 39:109–115

    Article  CAS  Google Scholar 

  • Perler FB, Davis EO, Dean GE, Gimble FS, Jack WE, Neff N, Noren CJ, Thorner J, Belfort M (1994) Protein splicing elements: inteins and exteins–a definition of terms and recommended nomenclature. Nucleic Acids Res 22:1125–1127

    Article  CAS  Google Scholar 

  • Pierce AJ, Hu P, Han M, Ellis N, Jasin M (2001) Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev 15:3237–3242

    Article  CAS  Google Scholar 

  • Porteus MH (2006) Mammalian gene targeting with designed zinc finger nucleases. Mol Ther 13:438–446

    Article  CAS  Google Scholar 

  • Porteus MH, Baltimore D (2003) Chimeric nucleases stimulate gene targeting in human cells. Science 300:763

    Article  Google Scholar 

  • Porteus MH, Cathomen T, Weitzman MD, Baltimore D (2003) Efficient gene targeting mediated by adeno-associated virus and DNA double-strand breaks. Mol Cell Biol 23:3558–3565

    Article  CAS  Google Scholar 

  • Posfai G, Kolisnychenko V, Bereczki Z, Blattner FR (1999) Markerless gene replacement in Escherichia coli stimulated by a double-strand break in the chromosome. Nucleic Acids Res 27:4409–4415

    Article  CAS  Google Scholar 

  • Poteete AR (2001) What makes the bacteriophage lambda Red system useful for genetic engineering: molecular mechanism and biological function. FEMS Microbiol Lett 201:9–14

    Google Scholar 

  • Prieto J, Epinat JC, Redondo P, Ramos E, Padro D, Cedrone F, Montoya G, Paques F, Blanco FJ (2008) Generation and analysis of mesophilic variants of the thermostable archaeal I-DmoI homing endonuclease. J Biol Chem 283:4364–4374

    Article  CAS  Google Scholar 

  • Puchta H (1999) Double-strand break-induced recombination between ectopic homologous sequences in somatic plant cells. Genetics 152:1173–1181

    CAS  Google Scholar 

  • Puchta H (1999) Use of I-Sce I to induce DNA double-strand breaks in Nicotiana. Methods Mol Biol 113:447–451

    Article  CAS  Google Scholar 

  • Puchta H (2002) Gene replacement by homologous recombination in plants. Plant Mol Biol 48:173–182

    Article  CAS  Google Scholar 

  • Puchta H, Dujon B, Hohn B (1996) Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc Natl Acad Sci U S A 93:5055–5060

    Article  CAS  Google Scholar 

  • Radecke F, Peter I, Radecke S, Gellhaus K, Schwarz K, Cathomen T (2006) Targeted chromosomal gene modification in human cells by single-stranded oligodeoxynucleotides in the presence of a DNA double-strand break. Mol Ther 14:798–808

    Article  CAS  Google Scholar 

  • Redondo P, Prieto J, Munoz IG, Alibes A, Stricher F, Serrano L, Cabaniols P, Daboussi F, Arnould S, Perez C, Duchateau P, Paques F, Blanco FJ, Montoya G (2008) Molecular basis of xeroderma pigmentosum group C DNA recognition by engineered meganucleases. Nature 456:107–111

    Article  CAS  Google Scholar 

  • Renfer E, Amon-Hassenzahl A, Steinmetz PR, Technau U (2010) A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc Natl Acad Sci U S A 107:104–108

    Article  CAS  Google Scholar 

  • Richardson C, Moynahan ME, Jasin M (1998) Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev 12:3831–3842

    Article  CAS  Google Scholar 

  • Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11:2600–2621

    Article  CAS  Google Scholar 

  • Romer P, Recht S, Lahaye T (2009) A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc Natl Acad Sci U S A 106:20526–20531

    Article  CAS  Google Scholar 

  • Rong YS, Golic KG (2000) Gene targeting by homologous recombination in Drosophila. Science 288:2013–2018

    Article  CAS  Google Scholar 

  • Rong YS, Golic KG (2001) A targeted gene knockout in Drosophila. Genetics 157:1307–1312

    Google Scholar 

  • Rong YS, Golic KG (2003) The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila. Genetics 165:1831–1842

    CAS  Google Scholar 

  • Rong YS, Titen SW, Xie HB, Golic MM, Bastiani M, Bandyopadhyay P, Olivera BM, Brodsky M, Rubin GM, Golic KG (2002) Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev 16:1568–1581

    Article  CAS  Google Scholar 

  • Rosen LE, Morrison HA, Masri S, Brown MJ, Springstubb B, Sussman D, Stoddard BL, Seligman LM (2006) Homing endonuclease I-CreI derivatives with novel DNA target specificities. Nucleic Acids Res 34:4791–4800

    Article  CAS  Google Scholar 

  • Rouet P, Smih F, 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

    CAS  Google Scholar 

  • Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK, Yeh JR (2011) Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 29:697–698

    Article  CAS  Google Scholar 

  • Scalley-Kim M, Mcconnell-Smith A, Stoddard BL (2007) Coevolution of a homing endonuclease and its host target sequence. J Mol Biol 372:1305–1319

    Article  CAS  Google Scholar 

  • Schaefer DG (2001) Gene targeting in Physcomitrella patens. Curr Opin Plant Biol 4:143–150

    Google Scholar 

  • Schaefer DG, Zryd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206

    Article  CAS  Google Scholar 

  • Schleifman EB, Chin JY, Glazer PM (2008) Triplex-mediated gene modification. Methods Mol Biol 435:175–190

    Article  CAS  Google Scholar 

  • Schmidt-Puchta W, Orel N, Kyryk A, Puchta H (2004) Intrachromosomal homologous recombination in Arabidopsis thaliana. Methods Mol Biol 262:25–34

    CAS  Google Scholar 

  • Scholze H, Boch J (2010) TAL effector-DNA specificity. Virulence 1:428–432

    Article  Google Scholar 

  • Seligman LM, Chisholm KM, Chevalier BS, Chadsey MS, Edwards ST, Savage JH, Veillet AL (2002) Mutations altering the cleavage specificity of a homing endonuclease. Nucleic Acids Res 30:3870–3879

    Article  CAS  Google Scholar 

  • Sethuraman J, Majer A, Friedrich NC, Edgell DR, Hausner G (2009) Genes within genes: multiple LAGLIDADG homing endonucleases target the ribosomal protein S3 gene encoded within an rnl group I intron of Ophiostoma and related taxa. Mol Biol Evol 26:2299–2315

    Article  CAS  Google Scholar 

  • Shen BW, Landthaler M, Shub DA, Stoddard BL (2004) DNA binding and cleavage by the HNH homing endonuclease I-HmuI. J Mol Biol 342:43–56

    Article  CAS  Google Scholar 

  • Siebert R, Puchta H (2002) Efficient repair of genomic double-strand breaks by homologous recombination between directly repeated sequences in the plant genome. Plant Cell 14:1121–1131

    Article  CAS  Google Scholar 

  • Silva G, Poirot L, Galetto R, Smith J, Montoya G, Duchateau P, Paques F (2011) Meganucleases and other tools for targeted genome engineering: perspectives and challenges for gene therapy. Curr Gene Ther 11:11–27

    Article  CAS  Google Scholar 

  • Silva GH, Belfort M, Wende W, Pingoud A (2006) From monomeric to homodimeric endonucleases and back: engineering novel specificity of LAGLIDADG enzymes. J Mol Biol 361:744–754

    Article  CAS  Google Scholar 

  • Silva GH, Dalgaard JZ, Belfort M, van Roey P (1999) Crystal structure of the thermostable archaeal intron-encoded endonuclease I-DmoI. J Mol Biol 286:1123–1136

    Article  CAS  Google Scholar 

  • Simon P, Cannata F, Perrouault L, Halby L, Concordet JP, Boutorine A, Ryabinin V, Sinyakov A, Giovannangeli C (2008) Sequence-specific DNA cleavage mediated by bipyridine polyamide conjugates. Nucleic Acids Res 36:3531–3538

    Article  CAS  Google Scholar 

  • Smih F, Rouet P, Romanienko PJ, Jasin M (1995) Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucleic Acids Res 23:5012–5019

    Article  CAS  Google Scholar 

  • Smith GR, Amundsen SK, Dabert P, Taylor AF (1995) The initiation and control of homologous recombination in Escherichia coli. Philos Trans R Soc Lond B Biol Sci 347:13–20

    Article  CAS  Google Scholar 

  • Smith J, Grizot S, Arnould S, Duclert A, Epinat JC, Chames P, Prieto J, Redondo P, Blanco FJ, Bravo J, Montoya G, Paques F, Duchateau P (2006) A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Res 34:e149

    Article  CAS  Google Scholar 

  • Smithies O (2001) Forty years with homologous recombination. Nat Med 7:1083–1086

    Article  CAS  Google Scholar 

  • Soldner F, Laganiere J, Cheng AW, Hockemeyer D, Gao Q, Alagappan R, Khurana V, Golbe LI, Myers RH, Lindquist S, Zhang L, Guschin D, Fong LK, Vu BJ, Meng X, Urnov FD, Rebar EJ, Gregory PD, Zhang HS, Jaenisch R (2011) Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 146:318–331

    Article  CAS  Google Scholar 

  • Spear MA (2000) Efficient DNA subcloning through selective restriction endonuclease digestion. Biotechniques 28:660–662, 664, 666 passim

    Google Scholar 

  • Spiegel PC, Chevalier B, Sussman D, Turmel M, Lemieux C, Stoddard BL (2006) The structure of I-CeuI homing endonuclease: evolving asymmetric DNA recognition from a symmetric protein scaffold. Structure 14:869–880

    Article  CAS  Google Scholar 

  • Stoddard BL (2005) Homing endonuclease structure and function. Q Rev Biophys 38:49–95

    Article  CAS  Google Scholar 

  • Stoddard BL, Scharenberg AM, Monnat RJ (2007) Advances in engineering homing endonucleases for gene targeting: ten years after structures. In: Bertolotti R, Ozawa K (eds) Progress in gene therapy: autologous and cancer stem cell gene therapy. World Scientific Publishing Co. Pte. Ltd., pp 135–168

    Chapter  Google Scholar 

  • Sussman D, Chadsey M, Fauce S, Engel A, Bruett A, Monnat R Jr, Stoddard BL, Seligman LM (2004) Isolation and characterization of new homing endonuclease specificities at individual target site positions. J Mol Biol 342:31–41

    Article  CAS  Google Scholar 

  • Suzuki N, Nonaka H, Tsuge Y, Okayama S, Inui M, Yukawa H (2005) Multiple large segment deletion method for Corynebacterium glutamicum. Appl Microbiol Biotechnol 69:151–161

    Article  CAS  Google Scholar 

  • Szczepek M, Brondani V, Buchel J, Serrano L, Segal DJ, Cathomen T (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25:786–793

    Article  CAS  Google Scholar 

  • Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination. Cell 33:25–35

    Article  CAS  Google Scholar 

  • Taghian DG, Nickoloff JA (1997) Chromosomal double-strand breaks induce gene conversion at high frequency in mammalian cells. Mol Cell Biol 17:6386–6393

    CAS  Google Scholar 

  • Takeuchi H, Georgiev O, Fetchko M, Kappeler M, Schaffner W, Egli D (2007) In vivo construction of transgenes in Drosophila. Genetics 175:2019–2028

    Article  CAS  Google Scholar 

  • Ten Asbroek AL, Ouellette M, Borst P (1990) Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature 348:174–175

    Article  Google Scholar 

  • Tesson L, Usal C, Menoret S, Leung E, Niles BJ, Remy S, Santiago Y, Vincent AI, Meng X, Zhang L, Gregory PD, Anegon I, Cost GJ (2011) Knockout rats generated by embryo microinjection of TALENs. Nat Biotechnol 29:695–696

    Article  CAS  Google Scholar 

  • Thermes V, Grabher C, Ristoratore F, Bourrat F, Choulika A, Wittbrodt J, Joly JS (2002) I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev 118:91–98

    Article  CAS  Google Scholar 

  • Thierry A, Dujon B (1992) Nested chromosomal fragmentation in yeast using the meganuclease I-Sce I: a new method for physical mapping of eukaryotic genomes. Nucleic Acids Res 20:5625–5631

    Article  CAS  Google Scholar 

  • Thomas KR, Capecchi MR (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51:503–512

    Article  CAS  Google Scholar 

  • Thomas KR, Capecchi MR (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346:847–850

    Article  CAS  Google Scholar 

  • Thyme SB, Jarjour J, Takeuchi R, Havranek JJ, Ashworth J, Scharenberg AM, Stoddard BL, Baker D (2009) Exploitation of binding energy for catalysis and design. Nature 461:1300–1304

    Article  CAS  Google Scholar 

  • Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445

    Article  CAS  Google Scholar 

  • Traver BE, Anderson MA, Adelman ZN (2009) Homing endonucleases catalyze double-stranded DNA breaks and somatic transgene excision in Aedes aegypti. Insect Mol Biol 18:623–633

    Article  CAS  Google Scholar 

  • Ulge UY, Baker DA, Monnat RJ Jr (2011) Comprehensive computational design of mCreI homing endonuclease cleavage specificity for genome engineering. Nucleic Acids Research 39:4330–4339

    Article  CAS  Google Scholar 

  • Urnov FD, Miller JC, Lee YL, Beausejour CM, Rock JM, Augustus S, Jamieson AC, Porteus MH, Gregory PD, Holmes MC (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435:646–651

    Article  CAS  Google Scholar 

  • van Roey P, Meehan L, Kowalski JC, Belfort M, Derbyshire V (2002) Catalytic domain structure and hypothesis for function of GIY-YIG intron endonuclease I-TevI. Nat Struct Biol 9:806–811

    Google Scholar 

  • van Roey P, Waddling CA, Fox KM, Belfort M, Derbyshire V (2001) Intertwined structure of the DNA-binding domain of intron endonuclease I-TevI with its substrate. EMBO J 20:3631–3637

    Article  Google Scholar 

  • Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S (2011) A modular cloning system for standardized assembly of multigene constructs. PLoS One 6:e16765

    Article  CAS  Google Scholar 

  • Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H, Ulge UY, Hovde BT, Baker D, Monnat RJ Jr, Burt A, Crisanti A (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473:212–215

    Article  CAS  Google Scholar 

  • Windbichler N, Papathanos PA, Catteruccia F, Ranson H, Burt A, Crisanti A (2007) Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Res 35:5922–5933

    Article  CAS  Google Scholar 

  • Yang M, Djukanovic V, Stagg J, Lenderts B, Bidney D, Falco SC, Lyznik LA (2009) Targeted mutagenesis in the progeny of maize transgenic plants. Plant Mol Biol 70:669–679

    Article  CAS  Google Scholar 

  • Young JJ, Cherone JM, Doyon Y, Ankoudinova I, Faraji FM, Lee AH, Ngo C, Guschin DY, Paschon DE, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Harland RM, Zeaitler B (2011) Efficient targeted gene disruption in the soma and germ line of the frog Xenopus tropicalis using engineered zinc-finger nucleases. Proc Natl Acad Sci U S A 108:7052–7057

    Article  CAS  Google Scholar 

  • Zhang F, Cong L, Lodato S, Kosuri S, Church GM, Arlotta P (2011) Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat Biotechnol 29:149–153

    Article  CAS  Google Scholar 

  • Zhao L, Bonocora RP, Shub DA, Stoddard BL (2007) The restriction fold turns to the dark side: a bacterial homing endonuclease with a PD-(D/E)-XK motif. EMBO J 26:2432–2442

    Article  CAS  Google Scholar 

  • Zou J, Maeder ML, Mali P, Pruett-Miller SM, Thibodeau-Beganny S, Chou BK, Chen G, Ye Z, Park IH, Daley GQ, Porteus MH, Joung JK, Cheng L (2009) Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 5:97–110

    Article  CAS  Google Scholar 

  • Zou J, Sweeney CL, Chou BK, Choi U, Pan J, Wang H, Dowey SN, Cheng L, Malech HL (2011) Oxidase deficient neutrophils from X-linked chronic granulomatous disease iPS cells: functional correction by zinc finger nuclease mediated safe harbor targeting. Blood 117:5561–5572

    Article  CAS  Google Scholar 

  • Capecchi MR (2) Generating mice with targeted mutations. Nat Med 7:1086–1090

    Article  CAS  Google Scholar 

  • Cavalier-Smith T (1985) Selfish DNA and the origin of introns. Nature 315(6017):283–284

    Article  CAS  Google Scholar 

  • Cermak T, Doyle EL, Christian M, Wang L, Zhang Y, Schmidt C, Baller JA, Somia NV, Bogdanove AJ, Voytas DF (2011) Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 39(12):e82

    Article  CAS  Google Scholar 

  • Chames P, Epinat JC, Guillier S, Patin A, Lacroix E, Paques F (2005) In vivo selection of engineered homing endonucleases using double-strand break induced homologous recombination. Nucleic Acids Res 33:e178

    Article  CAS  Google Scholar 

  • Chen Z, Wen F, Sun N, Zhao H (2009) Directed evolution of homing endonuclease I-SceI with altered sequence specificity gzp [pii] 10.1093/protein/gzp. Protein Eng Des Sel PEDS 22:249–256

    Article  CAS  Google Scholar 

  • Chevalier B, Turmel M, Lemieux C, Monnat RJ Jr, Stoddard BL (2003) Flexible DNA target site recognition by divergent homing endonuclease isoschizomers I-CreI and I-MsoI. J Mol Biol 329:253–269

    Article  CAS  Google Scholar 

  • Chevalier BS, Kortemme T, Chadsey MS, Baker D, Monnat RJ, Stoddard BL (2002) Design, activity, and structure of a highly specific artificial endonuclease. Mol Cell 10:895–905

    Article  CAS  Google Scholar 

  • Chevalier BS, Monnat RJ Jr, Stoddard BL (2) The homing endonuclease I-CreI uses three metals, one of which is shared between the two active sites. Nat Struct Biol 8:312–316

    Article  CAS  Google Scholar 

  • Chevalier BS, Stoddard BL (2) Homing endonucleases: structural and functional insight into the catalysis of intron/intein mobility. Nucleic Acids Res 29:3757–3774

    Article  Google Scholar 

  • Chiurazzi M, Ray A, Viret JF, Perera R, Wang XH, Lloyd AM, Signer ER (1996) Enhancement of somatic intrachromosomal homologous recombination in Arabidopsis by the HO endonuclease. Plant Cell 8:2057–2066

    CAS  Google Scholar 

  • Choulika A, Perrin A, Dujon B, 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

    CAS  Google Scholar 

  • Christian M, Cermak T, Doyle EL, Schmidt C, Zhang F, Hummel A, Bogdanove AJ, Voytas DF (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186:757–761

    Article  CAS  Google Scholar 

  • Cohen-Tannoudji M, Robine S, Choulika A, Pinto D, El Marjou F, Babinet C, Louvard D, Jaisser F (1998) I-SceI-induced gene replacement at a natural locus in embryonic stem cells. Mol Cell Biol 18:1444–1448

    CAS  Google Scholar 

  • Colleaux L, D’auriol L, Galibert F, Dujon B (1988) Recognition and cleavage site of the intron-encoded omega transposase. Proc Natl Acad Sci U S A 85:6022–6026

    Article  CAS  Google Scholar 

  • Colleaux L, Rougeulle C, Avner P, Dujon B (1993) Rapid physical mapping of YAC inserts by random integration of I-Sce I sites. Hum Mol Genet 2:265–271

    Article  CAS  Google Scholar 

  • Cost GJ, Freyvert Y, Vafiadis A, Santiago Y, Miller JC, Rebar E, Collingwood TN, Snowden A, Gregory PD (2010) BAK and BAX deletion using zinc-finger nucleases yields apoptosis-resistant CHO cells. Biotechnol Bioeng 105:330–340

    Article  CAS  Google Scholar 

  • Cox MM, Layton SL, Jiang T, Cole K, Hargis BM, Berghman LR, Bottje WG, Kwon YM (2007) Scarless and site-directed mutagenesis in Salmonella enteritidis chromosome. BMC Biotechnol 7:59

    Article  CAS  Google Scholar 

  • Cradick TJ, Keck K, Bradshaw S, Jamieson AC, Mccaffrey AP (2010) Zinc-finger nucleases as a novel therapeutic strategy for targeting hepatitis B virus DNAs. Mol Ther 18:947–954

    Article  CAS  Google Scholar 

  • Daboussi F, Zaslavskiy M, Poirot L, Loperfido M, Gouble A, Guyot V, Leduc S, Galetto R, Grizot S, Oficjalska D, Perez C, Delacote F, Dupuy A, Chion-Sotinel I, Le Clerre D, Lebuhotel C, Danos O, Lemaire F, Oussedik K, Cedrone F, Epinat JC, Smith J, Dickson G, Popplewell L, Koo T, Vandendriessche T, Chuah MK, Duclert A, Duchateau P, Paques F (2012) Chromosomal context and epigenetic mechanisms control the efficacy of genome editing by rare-cutting designer endonucleases. Nucleic Acids Res. Epub Mar 29

    Google Scholar 

  • Doetschman T, Gregg RG, Maeda N, Hooper ML, Melton DW, Thompson S, Smithies O (1987) Targetted correction of a mutant HPRT gene in mouse embryonic stem cells. Nature 330:576–578

    Article  CAS  Google Scholar 

  • Donoho G, Jasin M, 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

    CAS  Google Scholar 

  • Doyon JB, Pattanayak V, Meyer CB, Liu DR (2006) Directed evolution and substrate specificity profile of homing endonuclease I-SceI. J Am Chem Soc 128:2477–2484

    Article  CAS  Google Scholar 

  • Doyon Y, Mccammon JM, Miller JC, Faraji F, Ngo C, Katibah GE, Amora R, Hocking TD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Amacher SL (2008) Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol 26:702–708

    Article  CAS  Google Scholar 

  • Duan X, Gimble FS, Quiocho FA (1997) Crystal structure of PI-SceI, a homing endonuclease with protein splicing activity. Cell 89:555–564

    Article  CAS  Google Scholar 

  • Eisenschmidt K, Lanio T, Simoncsits A, Jeltsch A, Pingoud V, Wende W, Pingoud A (2005) Developing a programmed restriction endonuclease for highly specific DNA cleavage. Nucleic Acids Res 33:7039–7047

    Article  CAS  Google Scholar 

  • Elliott B, Richardson C, Winderbaum J, Nickoloff JA, Jasin M (1998) Gene conversion tracts from double-strand break repair in mammalian cells. Mol Cell Biol 18:93–101

    CAS  Google Scholar 

  • Engler C, Kandzia R, Marillonnet S (2008) A one pot, one step, precision cloning method with high throughput capability. PLoS One 3:e3647

    Article  CAS  Google Scholar 

  • Epinat JC, Arnould S, Chames P, Rochaix P, Desfontaines D, Puzin C, Patin A, Zanghellini A, Paques F, Lacroix E (2003) A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells. Nucleic Acids Res 31:2952–2962

    Article  CAS  Google Scholar 

  • Fajardo-Sanchez E, Stricher F, Paques F, Isalan M, Serrano L (2008) Computer design of obligate heterodimer meganucleases allows efficient cutting of custom DNA sequences Nucleic Acids Res 36:2163–2173

    CAS  Google Scholar 

  • Flannagan RS, Linn T, Valvano MA (2008) A system for the construction of targeted unmarked gene deletions in the genus Burkholderia. Environ Microbiol 10:1652–1660

    Article  CAS  Google Scholar 

  • Flick KE, Jurica MS, Monnat RJ Jr, Stoddard BL (1998) DNA binding and cleavage by the nuclear intron-encoded homing endonuclease I-PpoI. Nature 394:96–101

    Article  CAS  Google Scholar 

  • Flisikowska T, Thorey IS, Offner S, Ros F, Lifke V, Zeitler B, Rottmann O, Vincent A, Zhang L, Jenkins S, Niersbach H, Kind AJ, Gregory PD, Schnieke AE, Platzer J (2011) Efficient immunoglobulin gene disruption and targeted replacement in rabbit using zinc finger nucleases. PLoS One 6:e21045

    Article  CAS  Google Scholar 

  • Friedhoff P, Franke I, Meiss G, Wende W, Krause KL, Pingoud A (1999) A similar active site for non-specific and specific endonucleases. Nat Struct Biol 6:112–113

    Article  CAS  Google Scholar 

  • Galetto R, Duchateau P, Paques F (2009) Targeted approaches for gene therapy and the emergence of engineered meganucleases. Expert Opin Biol Ther 9:1289–1303

    Article  CAS  Google Scholar 

  • Gao H, Smith J, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, Jantz D, Lyznik LA (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J 61:176–187

    Article  CAS  Google Scholar 

  • Geissler R, Scholze H, Hahn S, Streubel J, Bonas U, Behrens SE, Boch J (2011) Transcriptionnal Activators of Human genes with progammable DNA-specificity. PLoS ONE 6:e19509

    Article  CAS  Google Scholar 

  • Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, Jenkins SS, Wood A, Cui X, Meng X, Vincent A, Lam S, Michalkiewicz M, Schilling R, Foeckler J, Kalloway S, Weiler H, Menoret S, Anegon I, Davis GD, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jacob HJ, Buelow R (2009) Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325:433

    Article  CAS  Google Scholar 

  • Gimble FS (2000) Invasion of a multitude of genetic niches by mobile endonuclease genes. FEMS Microbiol Lett 185:99–107

    Article  CAS  Google Scholar 

  • Gimble FS, Moure CM, Posey KL (2003) Assessing the plasticity of DNA target site recognition of the PI-SceI homing endonuclease using a bacterial two-hybrid selection system. J Mol Biol 334:993–1008

    Article  CAS  Google Scholar 

  • Glover L, Mcculloch R, Horn D (2008) Sequence homology and microhomology dominate chromosomal double-strand break repair in African trypanosomes. Nucleic Acids Res 36:2608–2618

    Article  CAS  Google Scholar 

  • Gouble A, Smith J, Bruneau S, Perez C, Guyot V, Cabaniols JP, Leduc S, Fiette L, Ave P, Micheau B, Duchateau P, Paques F (2006) Efficient in toto targeted recombination in mouse liver by meganuclease-induced double-strand break. J Gene Med 8:616–622

    Article  CAS  Google Scholar 

  • Grabher C, Wittbrodt J (2008) Recent advances in meganuclease-and transposon-mediated transgenesis of medaka and zebrafish. Methods Mol Biol 461:521–539

    Article  CAS  Google Scholar 

  • Grizot S, Duclert A, Thomas S, Duchateau P, Paques F (2011) Context dependence between subdomains in the DNA binding interface of the I-CreI homing endonuclease. Nucleic Acids Res 39:6124–6136

    Article  CAS  Google Scholar 

  • Grizot S, Epinat JC, Thomas S, Duclert A, Rolland S, Paques F, Duchateau P (2010) Generation of redesigned homing endonucleases comprising DNA-binding domains derived from two different scaffolds. Nucleic Acids Res 38:2006–2018

    Article  CAS  Google Scholar 

  • Grizot S, Smith J, Daboussi F, Prieto J, Redondo P, Merino N, Villate M, Thomas S, Lemaire L, Montoya G, Blanco FJ, Paques F, Duchateau P (2009) Efficient targeting of a SCID gene by an engineered single-chain homing endonuclease. Nucleic Acids Res 37:5405–5419

    Article  CAS  Google Scholar 

  • Grosse S, Huot N, Mahiet C, Arnould S, Barradeau S, Clerre DL, Chion-Sotinel I, Jacqmarcq C, Chapellier B, Ergani A, Desseaux C, Cedrone F, Conseiller E, Paques F, Labetoulle M, Smith J (2011) Meganuclease-mediated inhibition of HSV1 infection in cultured cells. Mol Ther 19:694–702

    Article  CAS  Google Scholar 

  • Gurlebeck D, Szurek B, Bonas U (2005) Dimerization of the bacterial effector protein AvrBs3 in the plant cell cytoplasm prior to nuclear import. Plant J 42:175–187

    Article  CAS  Google Scholar 

  • Haber JE (1998) Mating-type gene switching in Saccharomyces cerevisiae. Annu Rev Genet 32:561–599

    Article  CAS  Google Scholar 

  • Hauschild J, Petersen B, Santiago Y, Queisser AL, Carnwath JW, Lucas-Hahn A, Zhang L, Meng X, Gregory PD, Schwinzer R, Cost GJ, Niemann H (2011) Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc Natl Acad Sci U S A 108:12013–12017

    Article  CAS  Google Scholar 

  • Heath PJ, Stephens KM, Monnat RJ Jr, Stoddard BL (1997) The structure of I-Crel, a group I intron-encoded homing endonuclease. Nat Struct Biol 4:468–476

    Article  CAS  Google Scholar 

  • Hinnen A, Hicks JB, Fink GR (1978) Transformation of yeast. Proc Natl Acad Sci U S A 75:1929–1933

    Article  CAS  Google Scholar 

  • Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, Dekelver RC, Katibah GE, Amora R, Boydston EA, Zeitler B, Meng X, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R (2009) Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol 27:851–857

    Article  CAS  Google Scholar 

  • Hockemeyer DWH, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, Zeitler B, Cherone JM, Meng X, Hinkley SJ, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R (2011) Genetic engineering of human pluripotent cells using TALE nucleases. Nature Biotechnol 29:731–734

    Article  CAS  Google Scholar 

  • Horzempa J, Shanks RM, Brown MJ, Russo BC, O’Dee DM, Nau GJ (2010) Utilization of an unstable plasmid and the I-SceI endonuclease to generate routine markerless deletion mutants in Francisella tularensis. J Microbiol Methods 80:106–108

    Article  CAS  Google Scholar 

  • Huang P, Xiao A, Zhou M, Zhu Z, Lin S, Zhang B (2011) Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 29:699–700

    Article  CAS  Google Scholar 

  • Jacquier A, Dujon B (1985) An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 41:383–394

    Article  CAS  Google Scholar 

  • Jarjour J, West-Foyle H, Certo MT, Hubert CG, Doyle L, Getz MM, Stoddard BL, Scharenberg AM (2009) High-resolution profiling of homing endonuclease binding and catalytic specificity using yeast surface display. Nucleic Acids Res 37:6871–6880

    Article  CAS  Google Scholar 

  • Jurica MS, Monnat RJ Jr, Stoddard BL (1998) DNA recognition and cleavage by the LAGLIDADG homing endonuclease I-CreI. Mol Cell 2:469–476

    Article  CAS  Google Scholar 

  • Koller BH, Smithies O (1989) Inactivating the beta 2-microglobulin locus in mouse embryonic stem cells by homologous recombination. Proc Natl Acad Sci U S A 86:8932–8935

    Article  CAS  Google Scholar 

  • Kostriken R, Strathern JN, Klar AJ, Hicks JB, Heffron F (1983) A site-specific endonuclease essential for mating-type switching in Saccharomyces cerevisiae. Cell 35:167–174

    Article  CAS  Google Scholar 

  • Kuhlmann UC, Moore GR, James R, Kleanthous C, Hemmings AM (1999) Structural parsimony in endonuclease active sites: should the number of homing endonuclease families be redefined? FEBS Lett 463:1–2

    Article  CAS  Google Scholar 

  • Lambowitz AM, Caprara MG, Zimmerly S, Perlman PS (1999) Group I and group II ribozymes as RNPs: clues to the past and guides to the future. In: The RNA world, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Li H, Pellenz S, Ulge U, Stoddard BL, Monnat RJ Jr (2009) Generation of single-chain LAGLIDADG homing endonucleases from native homodimeric precursor proteins. Nucleic Acids Res 37:1650–1662

    Article  CAS  Google Scholar 

  • Li T, Huang S, Jiang WZ, Wright D, Spalding MH, Weeks DP, Yang B (2011) TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 39:359–372

    Article  CAS  Google Scholar 

  • Li T, Huang S, Zhao X, Wright DA, Carpenter S, Spalding MH, Weeks DP, Yang B (2011) Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 39(14):6315–6325

    Article  CAS  Google Scholar 

  • Liang F, Han M, Romanienko PJ, Jasin M (1998) Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci U S A 95:5172–5177

    Article  CAS  Google Scholar 

  • Liu PQ, Chan EM, Cost GJ, Zhang L, Wang J, Miller JC, Guschin DY, Reik A, Holmes MC, Mott JE, Collingwood TN, Gregory PD (2010) Generation of a triple-gene knockout mammalian cell line using engineered zinc-finger nucleases. Biotechnol Bioeng 106:97–105

    CAS  Google Scholar 

  • Loeber J, Pan FC, Pieler T (2009) Generation of transgenic frogs. Methods Mol Biol 561:65–72

    Article  CAS  Google Scholar 

  • Loizos N, Silva GH, Belfort M (1996) Intron-encoded endonuclease I-TevII binds across the minor groove and induces two distinct conformational changes in its DNA substrate. J Mol Biol 255:412–424

    Article  CAS  Google Scholar 

  • Lombardo A, Genovese P, Beausejour CM, Colleoni S, Lee YL, Kim KA, Ando D, Urnov FD, Galli C, Gregory PD, Holmes MC, Naldini L (2007) Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery. Nat Biotechnol 25:1298–1306

    Article  CAS  Google Scholar 

  • Lucas P, Otis C, Mercier JP, Turmel M, Lemieux C (2) Rapid evolution of the DNA-binding site in LAGLIDADG homing endonucleases. Nucleic Acids Res 29:960–969

    Article  Google Scholar 

  • Maeder ML, Thibodeau-Beganny S, Osiak A, Wright DA, Anthony RM, Eichtinger M, Jiang T, Foley JE, Winfrey RJ, Townsend JA, Unger-Wallace E, Sander JD, Muller-Lerch F, Fu F, Pearlberg J, Gobel C, Dassie JP, Pruett-Miller SM, Porteus MH, Sgroi DC, Iafrate AJ, Dobbs D, Mccray PB Jr, Cathomen T, Voytas DF, Joung JK (2008) Rapid “open-source” engineering of customized zinc-finger nucleases for highly efficient gene modification. Mol Cell 31:294–301

    Article  CAS  Google Scholar 

  • Maggert KA, Gong WJ, Golic KG (2008) Methods for homologous recombination in Drosophila. Methods Mol Biol 420:155–174

    Article  CAS  Google Scholar 

  • Mahfouz MM, Li L, Shamimuzzaman M, Wibowo A, Fang X, Zhu JK (2011) De novo-engineered transcription activator-like effector (TALE) hybrid nuclease with novel DNA binding specificity creates double-strand breaks. Proc Natl Acad Sci U S A 108:2623–2628

    Article  CAS  Google Scholar 

  • Majumdar A, Muniandy PA, Liu J, Liu JL, Liu ST, Cuenoud B, Seidman MM (2008) Targeted gene knock in and sequence modulation mediated by a psoralen-linked triplex-forming oligonucleotide. J Biol Chem 283:11244–11252

    Article  CAS  Google Scholar 

  • Mansour SL, Thomas KR, Capecchi MR (1988) Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature 336:348–352

    Article  CAS  Google Scholar 

  • Marcaida MJ, Munoz IG, Blanco FJ, Prieto J, Montoya G (2010) Homing endonucleases: from basics to therapeutic applications. Cell Mol Life Sci 67:727–748

    Article  CAS  Google Scholar 

  • Marcaida MJ, Prieto J, Redondo P, Nadra AD, Alibes A, Serrano L, Grizot S, Duchateau P, Paques F, Blanco FJ, Montoya G (2008) Crystal structure of I-DmoI in complex with its target DNA provides new insights into meganuclease engineering. Proc Natl Acad Sci U S A 105:16888–16893

    Article  CAS  Google Scholar 

  • Mashimo T, Takizawa A, Voigt B, Yoshimi K, Hiai H, Kuramoto T, Serikawa T (2010) Generation of knockout rats with X-linked severe combined immunodeficiency (X-SCID) using zinc-finger nucleases. PLoS One 5:e8870

    Article  CAS  Google Scholar 

  • Mcconnell Smith A, Takeuchi R, Pellenz S, Davis L, Maizels N, Monnat RJ Jr, Stoddard BL (2009) Generation of a nicking enzyme that stimulates site-specific gene conversion from the I-AniI LAGLIDADG homing endonuclease. Proc Natl Acad Sci U S A 106:5099–5104

    Article  CAS  Google Scholar 

  • Meng X, Noyes MB, Zhu LJ, Lawson ND, Wolfe SA (2008) Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol 26:695–701

    Article  CAS  Google Scholar 

  • Metzger MJ, Mcconnell-Smith A, Stoddard BL, Miller AD (2011) Single-strand nicks induce homologous recombination with less toxicity than double-strand breaks using an AAV vector template. Nucleic Acids Res 39:926–935

    Article  CAS  Google Scholar 

  • Miller DG, Petek LM, Russell DW (2003) Human gene targeting by adeno-associated virus vectors is enhanced by DNA double-strand breaks. Mol Cell Biol 23:3550–3557

    Article  CAS  Google Scholar 

  • Miller JC, Tan S, Qiao G, Barlow KA, Wang J, Xia DF, Meng X, Paschon DE, Leung E, Hinkley SJ, Dulay GP, Hua KL, Ankoudinova I, Cost GJ, Urnov FD, Zhang HS, Holmes MC, Zhang L, Gregory PD, Rebar EJ (2010) A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29:143–148

    Article  CAS  Google Scholar 

  • Morbitzer R, Elsaesser J, Hausner J, Lahaye T (2011) Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res 39(13):5790–5799

    Article  CAS  Google Scholar 

  • Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326:1501

    Article  CAS  Google Scholar 

  • Moure CM, Gimble FS, Quiocho FA (2002) Crystal structure of the intein homing endonuclease PI-SceI bound to its recognition sequence. Nat Struct Biol 9:764–770

    Article  CAS  Google Scholar 

  • Moure CM, Gimble FS, Quiocho FA (2003) The crystal structure of the gene targeting homing endonuclease I-SceI reveals the origins of its target site specificity. J Mol Biol 334:685–695

    Article  CAS  Google Scholar 

  • Moynahan ME, Jasin M (1997) Loss of heterozygosity induced by a chromosomal double-strand break. Proc Natl Acad Sci U S A 94:8988–8993

    Article  CAS  Google Scholar 

  • Munoz IG, Prieto J, Subramanian S, Coloma J, Redondo P, Villate M, Merino N, Marenchino M, D’Abramo M, Gervasio FL, Grizot S, Daboussi F, Smith J, Chion-Sotinel I, Paques F, Duchateau P, Alibes A, Stricher F, Serrano L, Blanco FJ, Montoya G (2011) Molecular basis of engineered meganuclease targeting of the endogenous human RAG1 locus. Nucleic Acids Res 39:729–743

    Article  CAS  Google Scholar 

  • Murphy KC (1998) Use of bacteriophage lambda recombination functions to promote gene replacement in Escherichia coli. J Bacteriol 180:2063–2071

    CAS  Google Scholar 

  • Mussolino C, Morbitzer R, Lutge F, Dannemann N, Lahaye T, Cathomen T (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39:9283–9293

    Article  CAS  Google Scholar 

  • Nickoloff JA, Chen EY, Heffron F (1986) A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc Natl Acad Sci U S A 83:7831–7835

    Article  CAS  Google Scholar 

  • Niu Y, Tenney K, Li H, Gimble FS (2008) Engineering variants of the I-SceI homing endonuclease with strand-specific and site-specific DNA-nicking activity. J Mol Biol 382:188–202

    Article  CAS  Google Scholar 

  • Nolan T, Papathanos P, Windbichler N, Magnusson K, Benton J, Catteruccia F, Crisanti A (2011) Developing transgenic anopheles mosquitoes for the sterile insect technique. Genetica 139:33–39

    Article  CAS  Google Scholar 

  • Ochiai H, Sakamoto N, Suzuki K, Akasaka K, Yamamoto T (2008) The Ars insulator facilitates I-SceI meganuclease-mediated transgenesis in the sea urchin embryo. Dev Dyn 237:2475–2482

    Article  CAS  Google Scholar 

  • Ogino H, Mcconnell WB, Grainger RM (2006) Highly efficient transgenesis in Xenopus tropicalis using I-SceI meganuclease. Mech Dev 123:103–113

    Article  CAS  Google Scholar 

  • Ogino H, Mcconnell WB, Grainger RM (2006) High-throughput transgenesis in Xenopus using I-SceI meganuclease. Nat Protoc 1:1703–1710

    Article  CAS  Google Scholar 

  • Orr-Weaver TL, Szostak JW, Rothstein RJ (1981) Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A 78:6354–6358

    Article  CAS  Google Scholar 

  • Orr-Weaver TL, Szostak JW, Rothstein RJ (1983) Genetic applications of yeast transformation with linear and gapped plasmids. Methods Enzymol 101:228–245

    Article  CAS  Google Scholar 

  • Pan FC, Chen Y, Loeber J, Henningfeld K, Pieler T (2006) I-SceI meganuclease-mediated transgenesis in Xenopus. Dev Dyn 235:247–252

    Article  CAS  Google Scholar 

  • Paques F, Duchateau P (2007) Meganucleases and DNA double-strand break-induced recombination: perspectives for gene therapy. Curr Gen Ther 7:49–66

    Article  CAS  Google Scholar 

  • Paques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63:349–404

    CAS  Google Scholar 

  • Perez C, Guyot V, Cabaniols JP, Gouble A, Micheaux B, Smith J, Leduc S, Paques F, Duchateau P (2005) Factors affecting double-strand break-induced homologous recombination in mammalian cells. Biotechniques 39:109–115

    Article  CAS  Google Scholar 

  • Perler FB, Davis EO, Dean GE, Gimble FS, Jack WE, Neff N, Noren CJ, Thorner J, Belfort M (1994) Protein splicing elements: inteins and exteins–a definition of terms and recommended nomenclature. Nucleic Acids Res 22:1125–1127

    Article  CAS  Google Scholar 

  • Pierce AJ, Hu P, Han M, Ellis N, Jasin M (2) Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev 15:3237–3242

    Article  CAS  Google Scholar 

  • Porteus MH (2006) Mammalian gene targeting with designed zinc finger nucleases. Mol Ther 13:438–446

    Article  CAS  Google Scholar 

  • Porteus MH, Baltimore D (2003) Chimeric nucleases stimulate gene targeting in human cells. Science 300:763

    Article  Google Scholar 

  • Porteus MH, Cathomen T, Weitzman MD, Baltimore D (2003) Efficient gene targeting mediated by adeno-associated virus and DNA double-strand breaks. Mol Cell Biol 23:3558–3565

    Article  CAS  Google Scholar 

  • Posfai G, Kolisnychenko V, Bereczki Z, Blattner FR (1999) Markerless gene replacement in Escherichia coli stimulated by a double-strand break in the chromosome. Nucleic Acids Res 27:4409–4415

    Article  CAS  Google Scholar 

  • Poteete AR (2) What makes the bacteriophage lambda Red system useful for genetic engineering: molecular mechanism and biological function. FEMS Microbiol Lett 201:9–14

    Google Scholar 

  • Prieto J, Epinat JC, Redondo P, Ramos E, Padro D, Cedrone F, Montoya G, Paques F, Blanco FJ (2008) Generation and analysis of mesophilic variants of the thermostable archaeal I-DmoI homing endonuclease. J Biol Chem 283:4364–4374

    Article  CAS  Google Scholar 

  • Puchta H (1999) Use of I-Sce I to induce DNA double-strand breaks in Nicotiana. Methods Mol Biol 113:447–451

    Article  CAS  Google Scholar 

  • Puchta H (1999) Double-strand break-induced recombination between ectopic homologous sequences in somatic plant cells. Genetics 152:1173–1181

    CAS  Google Scholar 

  • Puchta H (2002) Gene replacement by homologous recombination in plants. Plant Mol Biol 48:173–182

    Article  CAS  Google Scholar 

  • Puchta H, Dujon B, Hohn B (1996) Two different but related mechanisms are used in plants for the repair of genomic double-strand breaks by homologous recombination. Proc Natl Acad Sci U S A 93:5055–5060

    Article  CAS  Google Scholar 

  • Radecke F, Peter I, Radecke S, Gellhaus K, Schwarz K, Cathomen T (2006) Targeted chromosomal gene modification in human cells by single-stranded oligodeoxynucleotides in the presence of a DNA double-strand break. Mol Ther 14:798–808

    Article  CAS  Google Scholar 

  • Redondo P, Prieto J, Munoz IG, Alibes A, Stricher F, Serrano L, Cabaniols P, Daboussi F, Arnould S, Perez C, Duchateau P, Paques F, Blanco FJ, Montoya G (2008) Molecular basis of xeroderma pigmentosum group C DNA recognition by engineered meganucleases. Nature 456:107–111

    Article  CAS  Google Scholar 

  • Renfer E, Amon-Hassenzahl A, Steinmetz PR, Technau U (2010) A muscle-specific transgenic reporter line of the sea anemone, Nematostella vectensis. Proc Natl Acad Sci U S A 107:104–108

    Article  CAS  Google Scholar 

  • Richardson C, Moynahan ME, Jasin M (1998) Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev 12:3831–3842

    Article  CAS  Google Scholar 

  • Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Genes Dev 11:2600–2621

    Article  CAS  Google Scholar 

  • Romer P, Recht S, Lahaye T (2009) A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proc Natl Acad Sci U S A 106:20526–20531

    Article  CAS  Google Scholar 

  • Rong YS, Golic KG (2000) Gene targeting by homologous recombination in Drosophila. Science 288:2013–2018

    Article  CAS  Google Scholar 

  • Rong YS, Golic KG (2) A targeted gene knockout in Drosophila. Genetics 157:1307–1312

    Google Scholar 

  • Rong YS, Golic KG (2003) The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila. Genetics 165:1831–1842

    CAS  Google Scholar 

  • Rong YS, Titen SW, Xie HB, Golic MM, Bastiani M, Bandyopadhyay P, Olivera BM, Brodsky M, Rubin GM, Golic KG (2002) Targeted mutagenesis by homologous recombination in D. melanogaster. Genes Dev 16:1568–1581

    Article  CAS  Google Scholar 

  • Rosen LE, Morrison HA, Masri S, Brown MJ, Springstubb B, Sussman D, Stoddard BL, Seligman LM (2006) Homing endonuclease I-CreI derivatives with novel DNA target specificities. Nucleic Acids Res 34:4791–4800

    Article  CAS  Google Scholar 

  • Rothstein RJ (1983) One-step gene disruption in yeast. Methods Enzymol 101:202–211

    Article  CAS  Google Scholar 

  • Rouet P, Smih F, 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

    CAS  Google Scholar 

  • Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK, Yeh JR (2011) Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 29:697–698

    Article  CAS  Google Scholar 

  • Scalley-Kim M, Mcconnell-Smith A, Stoddard BL (2007) Coevolution of a homing endonuclease and its host target sequence. J Mol Biol 372:1305–1319

    Article  CAS  Google Scholar 

  • Schaefer DG (2) Gene targeting in Physcomitrella patens. Curr Opin Plant Biol 4:143–150

    Google Scholar 

  • Schaefer DG (2) Gene targeting in Physcomitrella patens. Curr Opin Plant Biol 4:143–150

    Article  Google Scholar 

  • Schaefer DG, Zryd JP (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J 11:1195–1206

    Article  CAS  Google Scholar 

  • Schleifman EB, Chin JY, Glazer PM (2008) Triplex-mediated gene modification. Methods Mol Biol 435:175–190

    Article  CAS  Google Scholar 

  • Schmidt-Puchta W, Orel N, Kyryk A, Puchta H (2004) Intrachromosomal homologous recombination in Arabidopsis thaliana. Methods Mol Biol 262:25–34

    CAS  Google Scholar 

  • Scholze H, Boch J (2010) TAL effector-DNA specificity. Virulence 1:428–432

    Article  Google Scholar 

  • Seligman LM, Chisholm KM, Chevalier BS, Chadsey MS, Edwards ST, Savage JH, Veillet AL (2002) Mutations altering the cleavage specificity of a homing endonuclease. Nucleic Acids Res 30:3870–3879

    Article  CAS  Google Scholar 

  • Sethuraman J, Majer A, Friedrich NC, Edgell DR, Hausner G (2009) Genes within genes: multiple LAGLIDADG homing endonucleases target the ribosomal protein S3 gene encoded within an rnl group I intron of Ophiostoma and related taxa. Mol Biol Evol 26:2299–2315

    Article  CAS  Google Scholar 

  • Shen BW, Landthaler M, Shub DA, Stoddard BL (2004) DNA binding and cleavage by the HNH homing endonuclease I-HmuI. J Mol Biol 342:43–56

    Article  CAS  Google Scholar 

  • Siebert R, Puchta H (2002) Efficient repair of genomic double-strand breaks by homologous recombination between directly repeated sequences in the plant genome. Plant Cell 14:1121–1131

    Article  CAS  Google Scholar 

  • Silva G, Poirot L, Galetto R, Smith J, Montoya G, Duchateau P, Paques F (2011) Meganucleases and other tools for targeted genome engineering: perspectives and challenges for gene therapy. Curr Gene Ther 11:11–27

    Article  CAS  Google Scholar 

  • Silva GH, Belfort M, Wende W, Pingoud A (2006) From monomeric to homodimeric endonucleases and back: engineering novel specificity of LAGLIDADG enzymes. J Mol Biol 361:744–754

    Article  CAS  Google Scholar 

  • Silva GH, Dalgaard JZ, Belfort M, van Roey P (1999) Crystal structure of the thermostable archaeal intron-encoded endonuclease I-DmoI. J Mol Biol 286:1123–1136

    Article  CAS  Google Scholar 

  • Simon P, Cannata F, Perrouault L, Halby L, Concordet JP, Boutorine A, Ryabinin V, Sinyakov A, Giovannangeli C (2008) Sequence-specific DNA cleavage mediated by bipyridine polyamide conjugates. Nucleic Acids Res 36:3531–3538

    Article  CAS  Google Scholar 

  • Smih F, Rouet P, Romanienko PJ, Jasin M (1995) Double-strand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucleic Acids Res 23:5012–5019

    Article  CAS  Google Scholar 

  • Smith GR, Amundsen SK, Dabert P, Taylor AF (1995) The initiation and control of homologous recombination in Escherichia coli. Philos Trans R Soc Lond B Biol Sci 347:13–20

    Article  CAS  Google Scholar 

  • Smith J, Grizot S, Arnould S, Duclert A, Epinat JC, Chames P, Prieto J, Redondo P, Blanco FJ, Bravo J, Montoya G, Paques F, Duchateau P (2006) A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Res 34:e149

    Article  CAS  Google Scholar 

  • Smithies O (2) Forty years with homologous recombination. Nat Med 7:1083–1086

    Article  CAS  Google Scholar 

  • Soldner F, Laganiere J, Cheng AW, Hockemeyer D, Gao Q, Alagappan R, Khurana V, Golbe LI, Myers RH, Lindquist S, Zhang L, Guschin D, Fong LK, Vu BJ, Meng X, Urnov FD, Rebar EJ, Gregory PD, Zhang HS, Jaenisch R (2011) Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 146:318–331

    Article  CAS  Google Scholar 

  • Spear MA (2000) Efficient DNA subcloning through selective restriction endonuclease digestion. Biotechniques 28:660–662, 664, 666 passim

    Google Scholar 

  • Spiegel PC, Chevalier B, Sussman D, Turmel M, Lemieux C, Stoddard BL (2006) The structure of I-CeuI homing endonuclease: evolving asymmetric DNA recognition from a symmetric protein scaffold. Structure 14:869–880

    Article  CAS  Google Scholar 

  • Stoddard BL (2005) Homing endonuclease structure and function. Q Rev Biophys 38:49–95

    Article  CAS  Google Scholar 

  • Stoddard BL, Scharenberg AM, Monnat RJ (2007) Advances in engineering homing endonucleases for gene targeting: ten years after structures. In: Bertolotti R, Ozawa K (eds) Progress in gene therapy: autologous and cancer stem cell gene therapy. World Scientific Publishing Co. Pte. Ltd., pp 135–168

    Chapter  Google Scholar 

  • Sussman D, Chadsey M, Fauce S, Engel A, Bruett A, Monnat R Jr, Stoddard BL, Seligman LM (2004) Isolation and characterization of new homing endonuclease specificities at individual target site positions. J Mol Biol 342:31–41

    Article  CAS  Google Scholar 

  • Suzuki N, Nonaka H, Tsuge Y, Okayama S, Inui M, Yukawa H (2005) Multiple large segment deletion method for Corynebacterium glutamicum. Appl Microbiol Biotechnol 69:151–161

    Article  CAS  Google Scholar 

  • Szczepek M, Brondani V, Buchel J, Serrano L, Segal DJ, Cathomen T (2007) Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 25:786–793

    Article  CAS  Google Scholar 

  • Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination. Cell 33:25–35

    Article  CAS  Google Scholar 

  • Taghian DG, Nickoloff JA (1997) Chromosomal double-strand breaks induce gene conversion at high frequency in mammalian cells. Mol Cell Biol 17:6386–6393

    CAS  Google Scholar 

  • Takeuchi H, Georgiev O, Fetchko M, Kappeler M, Schaffner W, Egli D (2007) In vivo construction of transgenes in Drosophila. Genetics 175:2019–2028

    Article  CAS  Google Scholar 

  • Ten Asbroek AL, Ouellette M, Borst P (1990) Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei. Nature 348:174–175

    Article  Google Scholar 

  • Tesson L, Usal C, Menoret S, Leung E, Niles BJ, Remy S, Santiago Y, Vincent AI, Meng X, Zhang L, Gregory PD, Anegon I, Cost GJ (2011) Knockout rats generated by embryo microinjection of TALENs. Nat Biotechnol 29:695–696

    Article  CAS  Google Scholar 

  • Thermes V, Grabher C, Ristoratore F, Bourrat F, Choulika A, Wittbrodt J, Joly JS (2002) I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech Dev 118:91–98

    Article  CAS  Google Scholar 

  • Thierry A, Dujon B (1992) Nested chromosomal fragmentation in yeast using the meganuclease I-Sce I: a new method for physical mapping of eukaryotic genomes. Nucleic Acids Res 20:5625–5631

    Article  CAS  Google Scholar 

  • Thomas KR, Capecchi MR (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51:503–512

    Article  CAS  Google Scholar 

  • Thomas KR, Capecchi MR (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346:847–850

    Article  CAS  Google Scholar 

  • Thyme SB, Jarjour J, Takeuchi R, Havranek JJ, Ashworth J, Scharenberg AM, Stoddard BL, Baker D (2009) Exploitation of binding energy for catalysis and design. Nature 461:1300–1304

    Article  CAS  Google Scholar 

  • Townsend JA, Wright DA, Winfrey RJ, Fu F, Maeder ML, Joung JK, Voytas DF (2009) High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 459:442–445

    Article  CAS  Google Scholar 

  • Traver BE, Anderson MA, Adelman ZN (2009) Homing endonucleases catalyze double-stranded DNA breaks and somatic transgene excision in Aedes aegypti. Insect Mol Biol 18:623–633

    Article  CAS  Google Scholar 

  • Ulge UY, Baker DA, Monnat RJ Jr (2011) Comprehensive computational design of mCreI homing endonuclease cleavage specificity for genome engineering. Nucleic Acids Research 39:4330–4339

    Article  CAS  Google Scholar 

  • Urnov FD, Miller JC, Lee YL, Beausejour CM, Rock JM, Augustus S, Jamieson AC, Porteus MH, Gregory PD, Holmes MC (2005) Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435:646–651

    Article  CAS  Google Scholar 

  • van Roey P, Meehan L, Kowalski JC, Belfort M, Derbyshire V (2002) Catalytic domain structure and hypothesis for function of GIY-YIG intron endonuclease I-TevI. Nat Struct Biol 9:806–811

    Google Scholar 

  • van Roey P, Waddling CA, Fox KM, Belfort M, Derbyshire V (2) Intertwined structure of the DNA-binding domain of intron endonuclease I-TevI with its substrate. EMBO J 20:3631–3637

    Article  Google Scholar 

  • Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S (2011) A modular cloning system for standardized assembly of multigene constructs. PLoS One 6:e16765

    Article  CAS  Google Scholar 

  • Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H, Ulge UY, Hovde BT, Baker D, Monnat RJ Jr, Burt A, Crisanti A (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473:212–215

    Article  CAS  Google Scholar 

  • Windbichler N, Papathanos PA, Catteruccia F, Ranson H, Burt A, Crisanti A (2007) Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucleic Acids Res 35:5922–5933

    Article  CAS  Google Scholar 

  • Yang M, Djukanovic V, Stagg J, Lenderts B, Bidney D, Falco SC, Lyznik LA (2009) Targeted mutagenesis in the progeny of maize transgenic plants. Plant Mol Biol 70:669–679

    Article  CAS  Google Scholar 

  • Young JJ, Cherone JM, Doyon Y, Ankoudinova I, Faraji FM, Lee AH, Ngo C, Guschin DY, Paschon DE, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Harland RM, Zeaitler B (2011) Efficient targeted gene disruption in the soma and germ line of the frog Xenopus tropicalis using engineered zinc-finger nucleases. Proc Natl Acad Sci U S A 108:7052–7057

    Article  CAS  Google Scholar 

  • Zhang F, Cong L, Lodato S, Kosuri S, Church GM, Arlotta P (2011) Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nat Biotechnol 29:149–153

    Article  CAS  Google Scholar 

  • Zhao L, Bonocora RP, Shub DA, Stoddard BL (2007) The restriction fold turns to the dark side: a bacterial homing endonuclease with a PD-(D/E)-XK motif. EMBO J 26:2432–2442

    Article  CAS  Google Scholar 

  • Zou J, Maeder ML, Mali P, Pruett-Miller SM, Thibodeau-Beganny S, Chou BK, Chen G, Ye Z, Park IH, Daley GQ, Porteus MH, Joung JK, Cheng L (2009) Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. Cell Stem Cell 5:97–110

    Article  CAS  Google Scholar 

  • Zou J, Sweeney CL, Chou BK, Choi U, Pan J, Wang H, Dowey SN, Cheng L, Malech HL (2011) Oxidase deficient neutrophils from X-linked chronic granulomatous disease iPS cells: functional correction by zinc finger nuclease mediated safe harbor targeting. Blood 117:5561–5572

    Article  CAS  Google Scholar 

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Epinat, J.C., Silva, G.H., Pâques, F., Smith, J., Duchateau, P. (2013). Engineered Meganucleases for Genome Engineering Purposes. In: Renault, S., Duchateau, P. (eds) Site-directed insertion of transgenes. Topics in Current Genetics, vol 23. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4531-5_6

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