Comprehensive homing endonuclease target site specificity profiling reveals evolutionary constraints and enables genome engineering applications

Nucleic Acids Research

Volumn 40, Issue 6, 2012, Pages 2587-2598

  Li, Hui ^a,b   Ulge, Umut Y ^a,b   Hovde, Blake T ^a   Doyle, Lindsey A ^c   Monnat, Raymond J ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL PROTEIN; HOMING ENDONUCLEASE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BASE PAIRING; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; GENETIC ENGINEERING; GREEN ALGA; HUMAN; HUMAN CELL; INTRON; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; STRUCTURAL HOMOLOGY;

ALGAE; CHLOROPHYTA;

EID: 84859311370     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1072     Document Type: Article

References (47)

1. Dujon, B. (1989) Group I introns as mobile genetic elements: facts and mechanistic speculations-a review. Gene, 82, 91-114 (Pubitemid 19248662)
2. Lambowitz, A.M. and Belfort, M. (1993) Introns as mobile genetic elements. Annu. Rev. Biochem., 62, 587-622 (Pubitemid 23237882)
3. Belfort, M. and Perlman, P.S. (1995) Mechanisms of intron mobility. J. Biol. Chem., 270, 30237-30240 (Pubitemid 26005064)
4. Belfort, M. (2005) Back to basics: structure, function, evolution and application of homing endonucleases and inteins. In: Belfort, M., Stoddard, B.L., Wood, D.W. and Derbyshire, V. (eds), Homing Endonucleases and Inteins. Springer-Verlag, Berlin, pp. 1-10
5. Stoddard, B.L. (2005) Homing endonuclease structure and function. Q. Rev. Biophys., 38, 1-47
6. Stoddard, B.L. (2011) Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure, 19, 7-15
7. Chevalier, B., Monnat, R.J. Jr and Stoddard, B.L. (2005) The LAGLIDADG homing endonuclease family. In: Belfort, M., Stoddard, B.L., Wood, D.W. and Derbyshire, V. (eds), Homing Endonucleases and Inteins. Springer-Verlag, Berlin, pp. 33-47
8. Grishin, A., Fonfara, I., Alexeevski, A., Spirin, S., Zanegina, O., Karyagina, A., Alexeyevsky, D. and Wende, W. (2010) Identification of conserved features of LAGLIDADG homing endonucleases. J. Bioinform. Computat. Biol., 8, 453-469
9. Colleaux, L., D'Auriol, L., Galibert, F. and Dujon, B. (1988) Recognition and cleavage site of the intron-encoded omega trnasposase. Proc. Natl Acad. Sci. USA, 85, 6022-6026
10. Argast, G.M., Stephens, K.M., Emond, M.J. and Monnat, R.J. 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 (Pubitemid 28327275)
11. Gimble, F.S. (2000) Invasion of a multitude of genetic niches by mobile endonuclease genes. FEMS Microbiol. Lett., 185, 99-107 (Pubitemid 30168983)
12. Burt, A. and Koufopanou, V. (2004) Homing endonuclease genes: the rise and fall and rise again of a selfish element. Curr. Opin. Genet. Dev., 14, 609-615 (Pubitemid 39505364)
13. Burt, A. and Trivers, R. (2006) Genes in Conflict: The Biology of Selfish Genetic Elements. The Belknap Press of Harvard University Press, Cambridge, MA
14. Goddard, M.R. and Burt, A. (1999) Recurrent invasion and extinction of a selfish gene. Proc. Natl Acad. Sci. USA, 96, 13880-13885
15. Thompson, A.J., Yuan, X., Kudlicki, W. and Herrin, D.L. (1992) Cleavage and recognition pattern of a double-strand-specific endonuclease (I-CreI) encoded by the chloroplast 23S rRNA intron of Chlamydomonas reinhardtii. Gene, 119, 247-251
16. Lucas, P., Otis, C., Mercier, J.P., Turmel, M. and Lemieux, C. (2001) Rapid evolution of the DNA-binding site in LAGLIDADG homing endonucleases. Nucleic Acids Res., 29, 960-969 (Pubitemid 32162265)
17. Jurica, M.S., Monnat, R.J. Jr and Stoddard, B.L. (1998) DNA recognition and cleavage by the LADLIDADG homing endonuclease I-CreI. Mol. Cell., 2, 469-476 (Pubitemid 128381299)
18. Chevalier, B., Turmel, M., Lemieux, C., Monnat, R.J. and Stoddard, B.L. (2003) Flexible DNA target site recognition by divergent homing endonuclease isoschizomers I-CreI and I-MsoI. J. Mol. Biol., 329, 253-269 (Pubitemid 36561582)
19. Li, H., Pellenz, S., Ulge, U., Stoddard, B.L. and Monnat, R.J. Jr (2009) Generation of single-chain LAGLIDADG homing endonucleases from native homodimeric precursor proteins. Nucleic Acids Res., 37, 1650-1662
20. Zhao, L., Pellenz, S. and Stoddard, B.L. (2009) Activity and specificity of the bacterial PD-(D/E)XK homing endonuclease I-Ssp6803I. J. Mol. Biol., 385, 1498-1510
21. Pierce, A.J., Johnson, R.D., Thompson, L.H. and Jasin, M. (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev., 13, 2633-2638 (Pubitemid 29508550)
22. Doyon, J.B., Pattanayak, V., Meyer, C.B. and Liu, D.R. (2006) Directed evolution and substrate specificity profile of homing endonuclease I-SceI. J. Am. Chem. Soc., 128, 2477-2484
23. Chen, C. and Okayama, H. (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol., 7, 2745-2752
24. Eastberg, J.H., Smith, A.M., Zhao, L., Ashworth, J., Shen, B.W. and Stoddard, B.L. (2007) Thermodynamics of DNA target site recognition by homing endonucleases. Nucleic Acids Res., 35, 7209-7221
25. Ulge, U.Y., Baker, D. and Monnat, R.J. Jr (2011) Comprehensive computational design of mCreI homing endonuclease cleavage specificity for genome engineering. Nucleic Acids Res., 39, 4330-4339
26. Burroughs, L., Woolfrey, A. and Shimamura, A. (2009) Shwachman-Diamond syndrome: a review of the clinical presentation, molecular pathogenesis, diagnosis, and treatment. Hematol. Oncol. Clin. North Am., 23, 233-248
27. Boocock, G.R.B., Morrison, J.A., Popovic, M., Richards, N., Ellis, L., Durie, P.R. and Rommens, J.M. (2003) Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat. Genet., 33, 97-101 (Pubitemid 36068690)
28. Belfort, M. and Roberts, R.J. (1997) Homing endonucleases: keeping the house in order. Nucleic Acids Res., 25, 3379-3388 (Pubitemid 27359210)
29. Arnould, S., Chames, P., Perez, C., Lacroix, E., Duclert, A., Epinat, J.C., Stricher, F., Petit, A.S., Patin, A., Guillier, S. et al. (2006) Engineering of large numbers of highly specific homing endonucleases that induce recombination on novel DNA targets. J. Mol. Biol., 355, 443-458 (Pubitemid 41785749)
30. Smith, J., Grizot, S., Arnould, S., Duclert, A., Epinat, J.C., Chames, P., Prieto, J., Redondo, P., Blanco, F.J., Bravo, J. et al. (2006) A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Res., 34, e149
31. Redondo, P., Prieto, J., Munoz, I.G., Alibes, A., Stricher, F., Serrano, L., Cabaniols, J.P., 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
32. Haugen, P., Simon, D.M. and Bhattacharya, D. (2005) The natural history of group I introns. Trends Genet., 21, 111-119 (Pubitemid 40127355)
33. Brosius, J., Dull, T.J. and Noller, H.F. (1980) Complete nucleotide sequence of the 23S ribosomal RNA gene from Escherichia coli. Proc. Natl Acad. Sci. USA, 77, 201-204 (Pubitemid 10142932)
34. Dunkle, J.A. and Cate, J.H. (2010) Ribosome structure and dynamics during translocation and termination. Annu. Rev. Biophys. Biomol. Struct., 39, 227-244
35. Ramakrishnan, V. (2010) Unraveling the structure of the ribosome (Nobel Lecture). Angewandte Chemie International Edition, 49, 4355-4380
36. Moore, P.B. and Steitz, T.A. (2011) The roles of RNA in the synthesis of protein. Cold Spring Harb. Perspect. Biol., 3, pii:a003780
37. Galburt, E.A., Chevalier, B., Tang, W., Jurica, M.S., Flick, K.E., Monnat, R.J. Jr and Stoddard, B.L. (1999) A novel endonuclease mechanism directly visualized for I-PpoI. Nat. Struct. Biol., 6, 1096-1099
38. Sato, N.S., Hirabayashi, N., Agmon, I., Yonath, A. and Suzuki, T. (2006) Comprehensive genetic selection revealed essential bases in the peptidyl-transferase center. Proc. Natl Acad. Sci. USA, 103, 15386-15391 (Pubitemid 44625601)
39. Spiegel, P.C., Chevalier, B., Sussman, D., Turmel, M., Lemieux, C. and Stoddard, B.L. (2006) The structure of I-CeuI homing endonuclease: evolving asymmetric DNA recognition from a symmetric protein scaffold. Structure, 14, 869-880
40. Gogarten, J.P. and Hilario, E. (2006) Inteins, introns, and homing endonucleases: recent revelations about the life cycle of parasitic genetic elements. BMC Evol. Biol., 6, 94
41. Stoddard, B. and Belfort, M. (2010) Social networking between mobile introns and their host genes. Mol. Microbiol., 78, 1-4
42. Seligman, L.M., Stephens, K.M., Savage, J.H. and Monnat, R.J. Jr (1997) Genetic analysis of the Chlamydomonas reinhardtii I-CreI mobile intron homing system in Escherichia coli. Genetics, 147, 1653-1664
43. Gimble, F.S., Moure, C.M. and Posey, K.L. (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 (Pubitemid 37485685)
44. Jacquier, A. and 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 (Pubitemid 16219410)
45. Gimble, F.S. and Thorner, J. (1992) Homing of a DNA endonuclease gene by meiotic gene conversion in Saccharomyces cerevisiae. Nature, 357, 301-306
46. Windbichler, N., Papathanos, P.A., Catteruccia, F., Ranson, H., Burt, A. and Crisanti, A. (2007) Homing endonuclease mediated gene targeting in Anopheles gambiae cells and embryos. Nucl. Acids Res., 35, 5922-5933 (Pubitemid 47506306)
47. Windbichler, N., Menichelli, M., Papathanos, P.A., Thyme, S.B., Li, H., Ulge, U.Y., Hovde, B.T., Baker, D., Monnat, R.J., Burt, A. et al. (2011) A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature, 473, 212-215.