Homing endonucleases: From genetic anomalies to programmable genomic clippers

Methods in Molecular Biology

Volumn 1123, Issue , 2014, Pages 1-26

  Belfort, Marlene ^a   Bonocora, Richard P ^b  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b WADSWORTH CENTER   (United States)

Author keywords

Altered specificity endonucleases; Biotechnology; Endonuclease applications; Genome editing; Homing endonucleases

Indexed keywords

ENDONUCLEASE;

ARTICLE; CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT; CRYSTAL STRUCTURE; DNA CLEAVAGE; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVE SITE; EXCISION REPAIR; GENE CONTROL; GENE CONVERSION; GENE DISRUPTION; GENE TARGETING; GENOME; GENOMIC INSTABILITY; GENOMICS; HOMOLOGOUS RECOMBINATION; HYDROGEN BOND; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RNA FOLDING; VECTOR CONTROL;

ENDONUCLEASES; EVOLUTION, MOLECULAR; GENE TARGETING; GENETIC ENGINEERING; MULTIGENE FAMILY; RNA EDITING;

EID: 84934440889     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-62703-968-0_1     Document Type: Article

References (158)

1. Netter P, Petrochilo E, Slonimski PP, Bolotin-Fukuhara M, Coen D, Deutsch J, Dujon B (1974) Mitochondrial genetics. VII. Allelism and mapping studies of ribosomal mutants resistant to chloramphenicol, erythromycin and spiramycin in S. Cerevisiae. Genetics 78:1063-1100
2. Bolotin M, Coen D, Deutsch J, Dujon B, Netter P, Petrochilo E, Slonimski PP (1971) La recombinaison des mitochondries chez Saccharomyces cerevisiae. Bull Inst Pasteur 69:215-239
3. Bos JL, Heyting C, Borst P, Arnberg AC, van Bruggen EFJ (1978) An insert in the single gene for the large ribosomal RNA in yeast mitochondrial DNA. Nature 275:336-338
4. Faye G, Dennebouy N, Kujawa C, Jacq C (1979) Inserted sequence in the mitochondrial 23S ribosomal RNA gene of the yeast Saccharomyces cerevisiae. Mol Gen Genet 168:101-109
5. Jacquier A, Dujon B (1985) An intronencoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 41:383-394
6. Lambowitz AM, Belfort M (1993) Introns as mobile genetic elements. Annu Rev Biochem 62:587-622
7. Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW (1983) The double-strand-break repair model for recombination. Cell 33:25-35
8. Belfort M (1990) Phage T4 introns: Selfsplicing and mobility. Annu Rev Genet 24:363-385
9. Dalgaard JZ, Garrett RA, Belfort M (1993) A site-specifi c endonuclease encoded by a typical archaeal intron. Proc Natl Acad Sci USA 90:5414-5417
10. Kane PM, Yamashiro CT, Wolczyk DF, Neff N, Goebl M, Stevens TH (1990) Protein splicing converts the yeast TFP1 gene product to the 69-kD subunit of the vacuolar H(+)-adenosine triphosphatase. Science 250:651-657
11. Hirata R, Oshumi Y, Nakano A, Kawasaki H, Suzuki K, Anraku Y (1990) Molecular structure of a gene, VMA1, encoding the catalytic subunit of H +-translocating adenosine triphosphatase from vacuolar membranes of Saccharomyces cerevisiae. J Biol Chem 265:6726-6733
12. Dalgaard JZ, Klar A, Moser MJ, Holley WR, Chatterjee A, Mian IS (1997) Statistical modeling and analysis of the LAGLIDADG family of site-specifi c endonucleases and identifi cation of an intein that encodes a site-specifi c endonuclease of the H-N-H family. Nucleic Acids Res 25:4626-4638
13. Sharma M, Ellis RL, Hinton DM (1992) Identifi cation of a family of bacteriophage T4 genes encoding proteins similar to those present in group I introns of fungi and phage. Proc Natl Acad Sci USA 89:6658-6662
14. Edgell DR, Shub DA (2001) Related homing endonucleases I-BmoI and I-TevI use different strategies to cleave homologous recognition sites. Proc Natl Acad Sci USA 98:7898-7903
15. Mota EM, Collins RA (1988) Independent evolution of structural and coding regions in a Neurospora mitochondrial intron. Nature 332:654-656
16. Quirk SM, Bell-Pedersen D, Belfort M (1989) Intron mobility in the T-Even phages: High frequency inheritance of group I introns promoted by intron open reading frames. Cell 56:455-465
17. Bonocora RP, Shub DA (2009) A likely pathway for formation of mobile group I introns. Curr Biol 19:223-228
18. Macreadie IG, Scott RM, Zinn AR, Butow RA (1985) Transposition of an intron in yeast mitochondria requires a protein encoded by that intron. Cell 41:395-402
19. Taylor GK, Stoddard BL (2012) Structural, functional and evolutionary relationships between homing endonucleases and proteins from their host organisms. Nucleic Acids Res 40:5189-5200
20. Haber JE, Wolfe KH (2005) Function and evolution of HO and VDE endonucleases in fungi. In: Belfort M, Derbyshire V, Stoddard BL, Wood DW (eds) Homing endonucleases and inteins. Springer, Berlin, pp 161-175
21. Pietrokovski S (1994) Conserved sequence features of inteins (protein introns) and their use in identifying new inteins and related proteins. Protein Sci 3:2340-2350
22. Gibb EA, Edgell DR (2010) Better late than never: Delayed translation of intron-encoded endonuclease I-TevI is required for effi cient splicing of its host group I intron. Mol Microbiol 78:35-46
23. Stoddard BL, Belfort M (2010) Social networking between mobile introns and their host genes. Mol Microbiol 78:1-4
24. Goddard MR, Burt A (1999) Recurrent invasion and extinction of a selfi sh gene. Proc Natl Acad Sci USA 96:13880-13885
25. Gimble FS (2000) Invasion of a multitude of genetic niches by mobile endonuclease genes. FEMS Microbiol Lett 185:99-107
26. Gogarten JP, Hilario E (2006) Inteins, introns, and homing endonucleases: Recent revelations about the life cycle of parasitic genetic elements. BMC Evol Biol 6:94
27. Liu Q, Belle A, Shub DA, Belfort M, Edgell DR (2003) SegG endonuclease promotes marker exclusion and mediates co-conversion from a distant cleavage site. J Mol Biol 334:13-23
28. Zeng Q, Bonocora RP, Shub DA (2009) A free-standing homing endonuclease targets an intron insertion site in the psbA gene of cyanophages. Curr Biol 19:218-222
29. Bonocora RP, Zeng Q, Abel EV, Shub DA (2011) A homing endonuclease and the 50-nt ribosomal bypass sequence of phage T4 constitute a mobile DNA cassette. Proc Natl Acad Sci USA 108:16351-16356
30. Loizos N, Tillier ERM, Belfort M (1994) Evolution of mobile group I introns: Recognition of intron sequences by an intron-encoded endonuclease. Proc Natl Acad Sci USA 91:11983-11987
31. Edgell DR, Stanger MJ, Belfort M (2004) Coincidence of cleavage sites of intron endonuclease I-TevI and critical sequences of the host thymidylate synthase gene. J Mol Biol 343:1231-1241
32. Koufopanou V, Goddard MR, Burt A (2002) Adaptation for horizontal transfer in a homing endonuclease. Mol Biol Evol 19:239-246
33. Stoddard BL (2011) Homing endonucleases: From microbial genetic invaders to reagents for targeted DNA modifi cation. Structure 19:7-15
34. Paques F, Duchateau P (2007) Meganucleases and DNA double-strand break-induced recombination: Perspectives for gene therapy. Curr Gene Ther 7:49-66
35. Colleaux L, D'Auriol L, Galibert F, Dujon B (1988) Recognition and cleavage site of the intron-encoded omega transposase. Proc Natl Acad Sci USA 85:6022-6026
36. Bryk M, Quirk SM, Mueller JE, Loizos N, Lawrence C, Belfort M (1993) The td intron endonuclease makes extensive sequence tolerant contacts across the minor groove of its DNA target. EMBO J 12:2141-2149
37. Pingoud A, Jeltsch A (2001) Structure and function of type II restriction endonucleases. Nucleic Acids Res 29:3705-3727
38. 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
39. Jurica MS, Monnat RJ Jr, Stoddard BL (1998) DNA recognition and cleavage by the LAGLIDADG homing endonuclease I-Cre I. Mol Cell 2:469-476
40. 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
41. Silva G, Dalgaard JZ, Belfort M, Van Roey P (1999) Crystal structure of the thermostable archaeal intron-encoded endonuclease I-Dmo I. J Mol Biol 286:1123-1136
42. Duan X, Gimble FS, Quiocho FA (1997) Crystal structure of PI-SceI, a homing endonuclease with protein splicing activity. Cell 89:555-564
43. Ichiyanagi K, Ishino Y, Ariyoshi M, Komori K, Morikawa K (2000) Crystal structure of an archaeal intron-encoded homing endonuclease PI-PfuI. J Mol Biol 300:889-901
44. Heath PJ, Stephens KM, Monnat RJ Jr, Stoddard BL (1997) The structure of I-Cre I, a group I intron-encoded homing endonuclease. Nat Struct Biol 4:468-476
45. Gimble FS, Stephens BW (1995) Substitutions in conserved dodecapeptide motifs that uncouple the DNA binding and DNA cleavage activities of PI-Sce I endonuclease. J Biol Chem 270:5849-5856
46. Schottler S, Wende W, Pingoud V, Pingoud A (2000) Identifi cation of Asp218 and Asp326 as the principal Mg2+ binding ligands of the homing endonuclease PI-SceI. Biochemistry 39:15895-15900
47. Chevalier BS, Monnat RJ Jr, Stoddard BL (2001) The homing endonuclease I-CreI uses three metals, one of which is shared between the two active sites. Nat Struct Biol 8:312-316
48. Chevalier B, Sussman D, Otis C, Noel AJ, Turmel M, Lemieux C, Stephens K, Monnat RJ Jr, Stoddard BL (2004) Metal-dependent DNA cleavage mechanism of the I-CreI LAGLIDADG homing endonuclease. Biochemistry 43:14015-14026
49. Klar AJ (2010) The yeast mating-type switching mechanism: A memoir. Genetics 186:443-449
50. 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
51. Ho Y, Kim SJ, Waring RB (1997) A protein encoded by a group I intron in Aspergillus nidulans directly assists RNA splicing and is a DNA endonuclease. Proc Natl Acad Sci USA 94:8994-8999
52. Wenzlau JM, Saldanha RJ, Butow RA, Perlman PS (1989) A latent intron-encoded maturase is also an endonuclease needed for intron mobility. Cell 56:421-430
53. Belfort M (2003) Two for the price of one: A bifunctional intron-encoded DNA endonuclease-RNA maturase. Genes Dev 17:2860-2863
54. Szczepanek T, Lazowska J (1996) Replacement of two non-adjacent amino acids in the S. Cerevisiae bi2 intron-encoded RNA maturase is suffi cient to gain a homingendonuclease activity. EMBO J 15:3758-3767
55. Chatterjee P, Brady KL, Solem A, Ho Y, Caprara MG (2003) Functionally distinct nucleic acid binding sites for a group I intron encoded RNA maturase/DNA homing endonuclease. J Mol Biol 329:239-251
56. Geese WJ, Kwon YK, Wen X, Waring RB (2003) In vitro analysis of the relationship between endonuclease and maturase activities in the bi-functional group I intron-encoded protein, I-AniI. Eur J Biochem 270:1543-1554
57. Knizewski L, Ginalski K (2007) Bacterial DUF199/COG1481 proteins including sporulation regulator WhiA are distant homologs of LAGLIDADG homing endonucleases that retained only DNA binding. Cell Cycle 6:1666-1670
58. Kaiser BK, Clifton MC, Shen BW, Stoddard BL (2009) The structure of a bacterial DUF199/WhiA protein: Domestication of an invasive endonuclease. Structure 17:1368-1376
59. Kaiser BK, Stoddard BL (2011) DNA recognition and transcriptional regulation by the WhiA sporulation factor. Sci Rep 1:156
60. Kowalski JC, Belfort M, Stapleton MA, Holpert M, Dansereau JT, Pietrokovski S, Baxter SM, Derbyshire V (1999) Confi guration of the catalytic GIY-YIG domain of intron endonuclease I-Tev I: Coincidence of computational and molecular fi ndings. Nucleic Acids Res 27:2115-2125
61. Dunin-Horkawicz S, Feder M, Bujnicki JM (2006) Phylogenomic analysis of the GIYYIG nuclease superfamily. BMC Genomics 7:98
62. Van Roey P, Meehan L, Kowalski J, Belfort M, Derbyshire V (2002) Catalytic domain structure and hypothesis for function of GIYYIG intron endonuclease I-TevI. Nat Struct Biol 9:806-811
63. Derbyshire V, Kowalski JC, Dansereau JT, Hauer CR, Belfort M (1997) Two-domain structure of the td intron-encoded endonuclease I-TevI correlates with the two-domain confi guration of the homing site. J Mol Biol 265:494-506
64. Liu QQ, Dansereau JT, Puttamadappa SS, Shekhtman A, Derbyshire V, Belfort M (2008) Role of the interdomain linker in distance determination for remote cleavage by homing endonuclease I-TevI. J Mol Biol 379:1094-1106
65. Liu Q-Q, Derbyshire V, Belfort M, Edgell DR (2006) Distance determination by GIYYIG intron endonucleases: Discrimination between repression and cleavage functions. Nucleic Acids Res 34:1755-1764
66. Bell-Pedersen D, Quirk SM, Bryk M, Belfort M (1991) I-TevI, the endonuclease encoded by the mobile td intron, recognizes binding and cleavage domains on its DNA target. Proc Natl Acad Sci USA 88:7719-7723
67. Belle A, Landthaler M, Shub DA (2002) Intronless homing: Site-specifi c endonuclease SegF of bacteriophage T4 mediates localized marker exclusion analogous to homing endonucleases of group I introns. Genes Dev 16:351-362
68. Mak AN, Lambert AR, Stoddard BL (2010) Folding, DNA recognition, and function of GIY-YIG endonucleases: Crystal structures of R.Eco29kI. Structure 18:1321-1331
69. Sokolowska M, Czapinska H, Bochtler M (2011) Hpy188I-DNA pre-and post-cleavage complexes-snapshots of the GIY-YIG nuclease mediated catalysis. Nucleic Acids Res 39:1554-1564
70. Pyatkov KI, Arkhipova IR, Malkova NV, Finnegan DJ, Evgen'ev MB (2004) Reverse transcriptase and endonuclease activities encoded by Penelope-like retroelements. Proc Natl Acad Sci USA 101:14719-14724
71. Edgell DR, Derbyshire V, Van Roey P, LaBonne S, Stanger MJ, Li Z, Boyd TM, Shub DA, Belfort M (2004) Intron-encoded homing endonuclease I-TevI also functions as a transcriptional autorepressor. Nat Struct Mol Biol 11:936-944
72. Ko T-P, Liao C-C, Ku W-Y, Chak K-F, Yuan HS (1999) The crystal structure of the DNase domain of colicin E7 in complex with its inhibitor lm7 protein. Structure 7:91-102
73. Kleanthous C, Kuhlmann UC, Pommer AJ, Ferguson N, Radford SE, Moore GR, James R, Hemmings AM (1999) Structural and mechanistic basis of immunity toward endonuclease colicins. Nat Struct Biol 6: 243-252
74. Friedhoff P, Franke I, Meiss G, Wende W, Krause KL, Pingoud A (1999) A similar active site for non-specifi c and specifi c endonucleases. Nat Struct Biol 6:112-113
75. Goodrich-Blair H, Shub DA (1996) Beyond homing: Competition between intron endonucleases confers a selective advantage on fl anking genetic markers. Cell 84:211-221
76. Landthaler M, Begley U, Lau NC, Shub DA (2002) Two self-splicing group I intron in the ribonucleotide reductase large subunit of Staphylococcus aureus phage Twort. Nucleic Acids Res 30:1935-1943
77. Robbins JB, Stapleton M, Smith D, Dansereau JT, Derbyshire V, Belfort M (2007) Homing endonuclease I-TevIII: Dimerization as a means to a double strand break. Nucleic Acids Res 35:1589-1600
78. Lambowitz AM, Zimmerly S (2011) Group II introns: Mobile ribozymes that invade DNA. Cold Spring Harb Perspect Biol 3:a003616
79. Gorbalenya AE (1994) Self-splicing group I and group II introns encode homologous (putative) DNA endonucleases of a new family. Protein Sci 3:1117-1120
80. Shub DA, Goodrich-Blair H, Eddy SR (1994) Amino acid sequence motif of group I intron endonucleases is conserved in open reading frames of group II introns. Trends Biochem Sci 19:402-404
81. Raaijmakers H, Toro I, Birkenbihl R, Kemper B, Suck D (2001) Conformational fl exibility in T4 endonuclease VII revealed by crystallography: Implications for substrate binding and cleavage. J Mol Biol 308:311-323
82. Bujnicki JM, Radlinska M, Rychlewski L (2001) Polyphyletic evolution of type II restriction enzymes revisited: Two independent sources of second-hand folds revealed. Trends Biochem Sci 26:9-11
83. Wiedenheft B, Sternberg SH, Doudna JA (2012) RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331-338
84. Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012) Cas9-crRNA ribonucleoprotein complex mediates specifi c DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci USA 109:E2579-E2586
85. Johansen S, Embley TM, Willassen NP (1993) A family of nuclear homing endonucleases. Nucleic Acids Res 21:4405
86. 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
87. 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 redefi ned FEBS Lett 463:1-2
88. Bujnicki JM (2003) Crystallographic and bioinformatic studies on restriction endonucleases: Inference of evolutionary relationships in the ?midnight zone? of homology. Curr Protein Pept Sci 4:327-337
89. Orlowski J, Boniecki M, Bujnicki JM (2007) I-Ssp6803I: The fi rst homing endonuclease from the PD-(D/E)XK superfamily exhibits an unusual mode of DNA recognition. Bioinformatics 23:527-530
90. Bonocora RP, Shub DA (2001) A novel group I intron-encoded endonuclease specifi c for the anticodon region of tRNA(fMet) genes. Mol Microbiol 39:1299-1306
91. Zhao L, Pellenz S, Stoddard BL (2009) Activity and specifi city of the bacterial PD-(D/E)XK homing endonuclease I-Ssp6803I. J Mol Biol 385:1498-1510
92. Steczkiewicz K, Muszewska A, Knizewski L, Rychlewski L, Ginalski K (2012) Sequence, structure and functional diversity of PD-(D/E)XK phosphodiesterase superfamily. Nucleic Acids Res 40:7016-7045
93. Rusch DB, Halpern AL, Sutton G, Heidelberg KB, Williamson S, Yooseph S, Wu D, Eisen JA, Hoffman JM, Remington K et al (2007) The Sorcerer II Global Ocean Sampling expedition: Northwest Atlantic through eastern tropical Pacifi c. PLoS Biol 5:e77
94. Yooseph S, Sutton G, Rusch DB, Halpern AL, Williamson SJ, Remington K, Eisen JA, Heidelberg KB, Manning G, Li W et al (2007) The Sorcerer II Global Ocean sampling expedition: Expanding the universe of protein families. PLoS Biol 5:e16
95. Taylor GK, Heiter DF, Pietrokovski S, Stoddard BL (2011) Activity, specifi city and structure of I-Bth0305I: A representative of a new homing endonuclease family. Nucleic Acids Res 39:9705-9719
96. Dassa B, London N, Stoddard BL, Schueler-Furman O, Pietrokovski S (2009) Fractured genes: A novel genomic arrangement involving new split inteins and a new homing endonuclease family. Nucleic Acids Res 37:2560-2573
97. Porteus MH, Carroll D (2005) Gene targeting using zinc fi nger nucleases. Nat Biotechnol 23:967-973
98. 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
99. Choulika A, Perrin A, Dujon B, Nicolas JF (1995) Induction of homologous recombination in mammalian chromosomes by using the I-Sce I system of Saccharomyces cerevisiae. Mol Cell Biol 15:1968-1973
100. 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
101. Seligman LM, Chisholm KM, Chevalier BS, Chadsey MS, Edwards ST, Savage JH, Veillet al (2002) Mutations altering the cleavage specifi city of a homing endonuclease. Nucleic Acids Res 30:3870-3879
102. Gruen M, Chang K, Serbanescu I, Liu DR (2002) An in vivo selection system for homing endonuclease activity. Nucleic Acids Res 30:e29
103. 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
104. 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
105. Jarjour J, West-Foyle H, Certo MT, Hubert CG, Doyle L, Getz MM, Stoddard BL, Scharenberg AM (2009) High-resolution profi ling of homing endonuclease binding and catalytic specifi city using yeast surface display. Nucleic Acids Res 37:6871-6880
106. Arnould S, Chames P, Perez C, Lacroix E, Duclert A, Epinat JC, Stricher F, Petit AS, Patin A, Guillier S et al (2006) Engineering of large numbers of highly specifi c homing endonucleases that induce recombination on novel DNA targets. J Mol Biol 355:443-458
107. Ashworth J, Havranek JJ, Duarte CM, Sussman D, Monnat R Jr, Stoddard BL, Baker D (2006) Computational redesign of endonuclease DNA binding and cleavage specifi city. Nature 441:656-659
108. Ulge UY, Baker DA, Monnat RJ Jr (2011) Comprehensive computational design of mCreI homing endonuclease cleavage specifi city for genome engineering. Nucleic Acids Res 39:4330-4339
109. Ashworth J, Taylor GK, Havranek JJ, Quadri SA, Stoddard BL, Baker D (2010) Computational reprogramming of homing endonuclease specifi city at multiple adjacent base pairs. Nucleic Acids Res 38:5601-5608
110. Takeuchi R, Lambert AR, Mak AN, Jacoby K, Dickson RJ, Gloor GB, Scharenberg AM, Edgell DR, Stoddard BL (2011) Tapping natural reservoirs of homing endonucleases for targeted gene modifi cation. Proc Natl Acad Sci USA 108:13077-13082
111. Jacoby K, Metzger M, Shen BW, Certo MT, Jarjour J, Stoddard BL, Scharenberg AM (2012) Expanding LAGLIDADG endonuclease scaffold diversity by rapidly surveying evolutionary sequence space. Nucleic Acids Res 40:4954-4964
112. Li H, Ulge UY, Hovde BT, Doyle LA, Monnat RJ Jr (2012) Comprehensive homing endonuclease target site specifi city profi ling reveals evolutionary constraints and enables genome engineering applications. Nucleic Acids Res 40:2587-2598
113. Mueller JE, Smith D, Bryk M, Belfort M (1995) Intron-encoded endonuclease I-TevI binds as a monomer to effect sequential cleavage via conformational changes in the td homing site. EMBO J 14:5724-5735
114. Carter JM, Friedrich NC, Kleinstiver B, Edgell DR (2007) Strand-specifi c contacts and divalent metal ion regulate double-strand break formation by the GIY-YIG homing endonuclease I-BmoI. J Mol Biol 374:306-321
115. Landthaler M, Shub DA (2003) The nicking homing endonuclease I-BasI is encoded by a group I intron in the DNA polymerase gene of the Bacillus thuringiensis phage Bastille. Nucleic Acids Res 31:3071-3077
116. Chan SH, Stoddard BL, Xu SY (2011) Natural and engineered nicking endonucleases-from cleavage mechanism to engineering of strand-specifi city. Nucleic Acids Res 39:1-18
117. 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-specifi c gene conversion from the I-AniI LAGLIDADG homing endonuclease. Proc Natl Acad Sci USA 106:5099-5104
118. 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
119. Chevalier BS, Kortemme T, Chadsey MS, Baker D, Monnat RJ, Stoddard BL (2002) Design, activity, and structure of a highly specifi c artifi cial endonuclease. Mol Cell 10:895-905
120. 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
121. Silva GH, Belfort M (2004) Analysis of the LAGLIDADG interface of the monomeric homing endonuclease I-DmoI. Nucleic Acids Res 32:3156-3168
122. Silva GH, Belfort M, Wende W, Pingoud A (2006) From monomeric to homodimeric endonucleases and back: Engineering novel specifi city of LAGLIDADG enzymes. J Mol Biol 361:744-754
123. Baxter S, Lambert AR, Kuhar R, Jarjour J, Kulshina N, Parmeggiani F, Danaher P, Gano J, Baker D, Stoddard BL et al (2012) Engineering domain fusion chimeras from I-OnuI family LAGLIDADG homing endonucleases. Nucleic Acids Res 40:7985-8000
124. 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
125. Fonfara I, Curth U, Pingoud A, Wende W (2012) Creating highly specifi c nucleases by fusion of active restriction endonucleases and catalytically inactive homing endonucleases. Nucleic Acids Res 40:847-860
126. Kleinstiver BP, Wolfs JM, Kolaczyk T, Roberts AK, Hu SX, Edgell DR (2012) Monomeric site-specifi c nucleases for genome editing. Proc Natl Acad Sci USA 109:8061-8066
127. Certo MT, Gwiazda KS, Kuhar R, Sather B, Curinga G, Mandt T, Brault M, Lambert AR, Baxter SK, Jacoby K et al (2012) Coupling endonucleases with DNA end-processing enzymes to drive gene disruption. Nat Methods 9:973-975
128. 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
129. 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
130. Cannon P, June C (2011) Chemokine receptor 5 knockout strategies. Curr Opin HIV AIDS 6:74-79
131. 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
132. Jasin M (1996) Genetic manipulation of genomes with rare-cutting endonucleases. Trends Genet 12:224-228
133. 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 effi cient gene correction in mammalian cells. J Mol Biol 371:49-65
134. Redondo P, Prieto J, Munoz IG, Alibes A, Stricher F, Serrano L, Cabaniols JP, Daboussi F, Arnould S, Perez C et al (2008) Molecular basis of xeroderma pigmentosum group C DNA recognition by engineered meganucleases. Nature 456:107-111
135. Grizot S, Smith J, Daboussi F, Prieto J, Redondo P, Merino N, Villate M, Thomas S, Lemaire L, Montoya G et al (2009) Effi cient targeting of a SCID gene by an engineered single-chain homing endonuclease. Nucleic Acids Res 37:5405-5419
136. Munoz IG, Prieto J, Subramanian S, Coloma J, Redondo P, Villate M, Merino N, Marenchino M, D'Abramo M, Gervasio FL et al (2011) Molecular basis of engineered meganuclease targeting of the endogenous human RAG1 locus. Nucleic Acids Res 39:729-743
137. Pessach IM, Notarangelo LD (2011) Gene therapy for primary immunodefi ciencies: Looking ahead, toward gene correction. J Allergy Clin Immunol 127:1344-1350
138. Chapdelaine P, Pichavant C, Rousseau J, Paques F, Tremblay JP (2010) Meganucleases can restore the reading frame of a mutated dystrophin. Gene Ther 17:846-858
139. Chan YS, Naujoks DA, Huen DS, Russell S (2011) Insect population control by homing endonuclease-based gene drive: An evaluation in Drosophila melanogaster. Genetics 188:33-44
140. Windbichler N, Menichelli M, Papathanos PA, Thyme SB, Li H, Ulge UY, Hovde BT, Baker D, Monnat RJ Jr, Burt A et al (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473:212-215
141. Klein TA, Windbichler N, Deredec A, Burt A, Benedict MQ (2012) Infertility resulting from transgenic I-PpoI male Anopheles gambiae in large cage trials. Pathog Glob Health 106:20-31
142. Deredec A, Godfray HC, Burt A (2011) Requirements for effective malaria control with homing endonuclease genes. Proc Natl Acad Sci USA 108:E874-E880
143. Gao H, Smith J, Yang M, Jones S, Djukanovic V, Nicholson MG, West A, Bidney D, Falco SC, Jantz D et al (2010) Heritable targeted mutagenesis in maize using a designed endonuclease. Plant J 61:176-187
144. Zeevi V, Liang Z, Arieli U, Tzfi ra T (2012) Zinc fi nger nuclease and homing endonucleasemediated assembly of multigene plant transformation vectors. Plant Physiol 158:132-144
145. Vainstein A, Marton I, Zuker A, Danziger M, Tzfi ra T (2011) Permanent genome modifi-cations in plant cells by transient viral vectors. Trends Biotechnol 29:363-369
146. Mak AN, Bradley P, Cernadas RA, Bogdanove AJ, Stoddard BL (2012) The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335:716-719
147. Deng D, Yan C, Pan X, Mahfouz M, Wang J, Zhu JK, Shi Y, Yan N (2012) Structural basis for sequence-specifi c recognition of DNA by TAL effectors. Science 335:720-723
148. Schiffer JT, Aubert M, Weber ND, Mintzer E, Stone D, Jerome KR (2012) Targeted DNA mutagenesis for the cure of chronic viral infections. J Virol 86:8920-8936
149. Meckler JF, Bhakta MS, Kim MS, Ovadia R, Habrian CH, Zykovich A, Yu A, Lockwood SH, Morbitzer R, Elsaesser J et al (2013) Quantitative analysis of TALE-DNA interactions suggests polarity effects. Nucleic Acids Res 41:4118-4128
150. Kim Y, Kweon J, Kim JS (2013) TALENs and ZFNs are associated with different mutation signatures. Nat Methods 10:185
151. Cui X, Davis G (2007) Mobile group II intron targeting: Applications in prokaryotes and perspectives in eukaryotes. Front Biosci 12:4972-4985
152. Burgess DJ (2013) Technology: A CRISPR genome-editing tool. Nat Rev Genet 14:80
153. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816-821
154. Mali P, Yang L, Esvelt KM, Aach J, Guell M, Dicarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823-826
155. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffi ni LA et al (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819-823
156. Cho SW, Kim S, Kim JM, Kim JS (2013) Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol 31:230-232
157. Hwang WY, Fu Y, Reyon D, Maeder ML, Tsai SQ, Sander JD, Peterson RT, Yeh JR, Joung JK (2013) Effi cient genome editing in zebrafi sh using a CRISPR-Cas system. Nat Biotechnol 31:227-229
158. Jiang W, Bikard D, Cox D, Zhang F, Marraffi ni LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31:223-239