Massively parallel determination and modeling of endonuclease substrate specificity

Nucleic Acids Research

Volumn 42, Issue 22, 2014, Pages 13839-13852

  Thyme, Summer B ^a   Song, Yifan ^b   Brunette, T J ^b   Szeto, Mindy D ^b   Kusak, Lara ^b   Bradley, Philip ^c   Baker, David ^b,d  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; DEOXYRIBONUCLEASE; DNA;

ARTICLE; CONTROLLED STUDY; DATA BASE; DNA CLEAVAGE; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GENOME; HIGH THROUGHPUT SCREENING; MODEL; PRIORITY JOURNAL; SEQUENCE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; DNA SEQUENCE; HIGH THROUGHPUT SEQUENCING; METABOLISM; NUCLEOTIDE SEQUENCE;

BACTERIA (MICROORGANISMS);

BASE SEQUENCE; COMPUTER SIMULATION; DNA; DNA CLEAVAGE; ENDODEOXYRIBONUCLEASES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MODELS, MOLECULAR; SEQUENCE ANALYSIS, DNA; SUBSTRATE SPECIFICITY;

EID: 84927662735     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1096     Document Type: Article

References (66)

1. Stoddard, B. L. (2011) Homing endonucleases: from microbial genetic invaders to reagents for targeted DNA modification. Structure, 19, 7-15.
2. Thyme, S. B., Jarjour, J., Takeuchi, R., Havranek, J. J., Ashworth, J., Scharenberg, A. M., Stoddard, B. L. and Baker, D. (2009) Exploitation of binding energy for catalysis and design. Nature, 461, 1300-1304.
3. Ashworth, J., Taylor, G. K., Havranek, J. J., Quadri, S. A., Stoddard, B. L. and Baker, D. (2010) Computational reprogramming of homing endonuclease specificity at multiple adjacent base pairs. Nucleic Acids Res., 38, 5601-5608.
4. Takeuchi, R., Lambert, A. R., Mak, A. N.-S., Jacoby, K., Dickson, R. J., Gloor, G. B., Scharenberg, A. M., Edgell, D. R. and Stoddard, B. L. (2011) Tapping natural reservoirs of homing endonucleases for targeted gene modification. Proc. Natl. Acad. Sci. U. S. A., 108, 13077-13082.
5. Redondo, P., Prieto, J., Muñoz, I. G., Alibés, 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.
6. Popplewell, L., Koo, T., Leclerc, X., Duclert, A., Mamchaoui, K., Gouble, A., Mouly, V., Voit, T., Pâques, F., Cédrone, F. et al. (2013) Gene correction of a duchenne muscular dystrophy mutation by meganuclease-enhanced exon knock-in. Hum. Gene Ther., 24, 692-701.
7. Djukanovic, V., Smith, J., Lowe, K., Yang, M., Gao, H., Jones, S., Nicholson, M. G., West, A., Lape, J., Bidney, D. et al. (2013) Male-sterile maize plants produced by targeted mutagenesis of the cytochrome P450-like gene (MS26) using a re-designed I-CreI homing endonuclease. Plant J., 76, 888-899.
8. Chan, Y. S., Takeuchi, R., Jarjour, J., Huen, D. S., Stoddard, B. L. and Russell, S. (2013) The design and in vivo evaluation of engineered i-onui-based enzymes for HEG gene drive. PLoS One, 8, e74254.
9. Szeto, M. D., Boissel, S. J. S., Baker, D. and Thyme, S. B. (2011) Mining endonuclease cleavage determinants in genomic sequence data. J. Biol. Chem., 286, 32617-32627.
10. Barzel, A., Privman, E., Peeri, M., Naor, A., Shachar, E., Burstein, D., Lazary, R., Gophna, U., Pupko, T. and Kupiec, M. (2011) Native homing endonucleases can target conserved genes in humans and in animal models. Nucleic Acids Res., 39, 6646-6659.
11. Baxter, S., Lambert, A. R., Kuhar, R., Jarjour, J., Kulshina, N., Parmeggiani, F., Danaher, P., Gano, J., Baker, D., Stoddard, B. L. et al. (2012) Engineering domain fusion chimeras from I-OnuI family LAGLIDADG homing endonucleases. Nucleic Acids Res., 40, 7985-8000.
12. Jacoby, K., Metzger, M., Shen, B. W., Certo, M. T., Jarjour, J., Stoddard, B. L. and Scharenberg, A. M. (2012) Expanding LAGLIDADG endonuclease scaffold diversity by rapidly surveying evolutionary sequence space. Nucleic Acids Res., 40, 4954-4964.
13. Molina, R., Redondo, P., Stella, S., Marenchino, M., D'Abramo, M., Gervasio, F. L., Epinat, J. C., Valton, J., Grizot, S., Duchateau, P. et al. (2012) Non-specific protein-DNA interactions control I-CreI target binding and cleavage. Nucleic Acids Res., 40, 6936-6945.
14. Thyme, S. B., Boissel, S. J. S., Arshiya Quadri, S., Nolan, T., Baker, D. A., Park, R. U., Kusak, L., Ashworth, J. and Baker, D. (2013) Reprogramming homing endonuclease specificity through computational design and directed evolution. Nucleic Acids Res., 42, 2564-2576.
15. Whitehead, T. A., Chevalier, A., Song, Y., Dreyfus, C., Fleishman, S. J., De Mattos, C., Myers, C. A., Kamisetty, H., Blair, P., Wilson, I. A. et al. (2012) Optimization of affinity, specificity and function of designed influenza inhibitors using deep sequencing. Nat. Biotechnol., 30, 543-548.
16. Starita, L. M., Pruneda, J. N., Lo, R. S., Fowler, D. M., Kim, H. J., Hiatt, J. B., Shendure, J., Brzovic, P. S., Fields, S. and Klevit, R. E. (2013) Activity-enhancing mutations in an E3 ubiquitin ligase identified by high-throughput mutagenesis. Proc. Natl. Acad. Sci. U. S. A., 110, E1263-E1272.
17. Fowler, D. M., Araya, C. L., Fleishman, S. J., Kellogg, E. H., Stephany, J. J., Baker, D. and Fields, S. (2010) High-resolution mapping of protein sequence-function relationships. Nat. Methods, 7, 741-746.
18. Araya, C. L. and Fowler, D. M. (2011) Deep mutational scanning: assessing protein function on a massive scale. Trends Biotechnol., 29, 435-442.
19. Maerkl, S. J. and Quake, S. R. (2007) A systems approach to measuring the binding energy landscapes of transcription factors. Science, 315, 233-237.
20. Kinney, J. B., Murugan, A., Callan, C. G. and Cox, E. C. (2010) Using deep sequencing to characterize the biophysical mechanism of a transcriptional regulatory sequence. Proc. Natl. Acad. Sci. U. S. A., 107, 9158-9163.
21. Jolma, A., Kivioja, T., Toivonen, J., Cheng, L., Wei, G., Enge, M., Taipale, M., Vaquerizas, J. M., Yan, J., Sillanpää, M. J. et al. (2010) Multiplexed massively parallel SELEX for characterization of human transcription factor binding specificities. Genome Res., 20, 861-873.
22. Wang, J., Lu, J., Gu, G. and Liu, Y. (2011) In vitro DNA-binding profile of transcription factors: methods and new insights. J. Endocrinol., 210, 15-27.
23. Geertz, M. and Maerkl, S. J. (2010) Experimental strategies for studying transcription factor-DNA binding specificities. Brief. Funct. Genomics, 9, 362-373.
24. Pattanayak, V., Lin, S., Guilinger, J. P., Ma, E., Doudna, J. A. and Liu, D. R. (2013) High-throughput profiling of off-target DNA cleavage reveals RNA-programmed Cas9 nuclease specificity. Nat. Biotechnol., 31, 839-843.
25. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
26. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. and Wheeler, D. L. (2005) GenBank. Nucleic Acids Res., 33, D34-D38.
27. Pruitt, K. D., Tatusova, T. and Maglott, D. R. (2007) NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res., 35, D61-D65.
28. Nomura, N., Nomura, Y., Sussman, D., Klein, D. and Stoddard, B. L. (2008) Recognition of a common rDNA target site in archaea and eukarya by analogous LAGLIDADG and His-Cys box homing endonucleases. Nucleic Acids Res., 36, 6988-6998.
29. Moure, C. M., Gimble, F. S. and Quiocho, F. A. (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.
30. 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.
31. Marcaida, M. J., Prieto, J., Redondo, P., Nadra, A. D., Alibés, A., Serrano, L., Grizot, S., Duchateau, P., Pâques, F., Blanco, F. J. et al. (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.
32. 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.
33. Scalley-Kim, M., McConnell-Smith, A. and Stoddard, B. L. (2007) Coevolution of a homing endonuclease and its host target sequence. J. Mol. Biol., 372, 1305-1319.
34. Bolduc, J. M., Spiegel, P. C., Chatterjee, P., Brady, K. L., Downing, M. E., Caprara, M. G., Waring, R. B. and Stoddard, B. L. (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.
35. Söding, J. (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics, 21, 951-960.
36. Crooks, G. E., Hon, G., Chandonia, J.-M. and Brenner, S. E. (2004) WebLogo: a sequence logo generator. Genome Res., 14, 1188-1190.
37. Schneider, T. D. and Stephens, R. M. (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res., 18, 6097-6100.
38. Van Der Walt, S., Colbert, S. C. and Varoquaux, G. (2011) The NumPy array: a structure for efficient numerical computation. Comput. Sci. Eng., 13, 22-30.
39. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 4673-4680.
40. Stemmer, W. P., Crameri, A., Ha, K. D., Brennan, T. M. and Heyneker, H. L. (1995) Single-step assembly of a gene and entire plasmid from large numbers of oligodeoxyribonucleotides. Gene, 164, 49-53.
41. Thyme, S. B., Baker, D. and Bradley, P. (2012) Improved modeling of side-chain-base interactions and plasticity in protein-DNA interface design. J. Mol. Biol., 419, 255-274.
42. 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.
43. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif., 41, 207-234.
44. Halford, S. E., Johnson, N. P. and Grinsted, J. (1980) The EcoRI restriction endonuclease with bacteriophage lambda DNA. Kinetic studies. Biochem. J., 191, 581-592.
45. Geese, W. J., Kwon, Y. K., Wen, X. and Waring, R. B. (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.
46. Song, Y., DiMaio, F., Wang, R. Y.-R., Kim, D., Miles, C., Brunette, T., Thompson, J. and Baker, D. (2013) High-resolution comparative modeling with RosettaCM. Structure, 21, 1735-1742.
47. Remmert, M., Biegert, A., Hauser, A. and Söding, J. (2012) HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat. Methods, 9, 173-175.
48. Yang, Y., Faraggi, E., Zhao, H. and Zhou, Y. (2011) Improving protein fold recognition and template-based modeling by employing probabilistic-based matching between predicted one-dimensional structural properties of query and corresponding native properties of templates. Bioinformatics, 27, 2076-2082.
49. Peng, J. and Xu, J. (2009) Boosting protein threading accuracy. Res. Comput. Mol. Biol., 5541, 31-45.
50. Zhang, Y. and Skolnick, J. (2005) TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res., 33, 2302-2309.
51. Thiéry, O., Börstler, B., Ineichen, K. and Redecker, D. (2010) Evolutionary dynamics of introns and homing endonuclease ORFs in a region of the large subunit of the mitochondrial rRNA in Glomus species (arbuscular mycorrhizal fungi, Glomeromycota). Mol. Phylogenet. Evol., 55, 599-610.
52. Cho, Y., Qiu, Y. L., Kuhlman, P. and Palmer, J. D. (1998) Explosive invasion of plant mitochondria by a group I intron. Proc. Natl. Acad. Sci. U. S. A., 95, 14244-14249.
53. Fukami, H., Chen, C. A., Chiou, C.-Y. and Knowlton, N. (2007) Novel group I introns encoding a putative homing endonuclease in the mitochondrial cox1 gene of Scleractinian corals. J. Mol. Evol., 64, 591-600.
54. Takeuchi, R., Certo, M., Caprara, M. G., Scharenberg, A. M. and Stoddard, B. L. (2009) Optimization of in vivo activity of a bifunctional homing endonuclease and maturase reverses evolutionary degradation. Nucleic Acids Res., 37, 877-890.
55. Longo, A., Leonard, C. W., Bassi, G. S., Berndt, D., Krahn, J. M., Hall, T. M. T. and Weeks, K. M. (2005) Evolution from DNA to RNA recognition by the bI3 LAGLIDADG maturase. Nat. Struct. Mol. Biol., 12, 779-787.
56. Lehmann, M., Loch, C., Middendorf, A., Studer, D., Lassen, S. F., Pasamontes, L., van Loon, A. P. G. M. and Wyss, M. (2002) The consensus concept for thermostability engineering of proteins: further proof of concept. Protein Eng., 15, 403-411.
57. Bershtein, S., Goldin, K. and Tawfik, D. S. (2008) Intense neutral drifits yield robust and evolvable consensus proteins. J. Mol. Biol., 379, 1029-1044.
58. Li, H., Ulge, U. Y., Hovde, B. T., Doyle, L. A. and Monnat, R. J. (2012) Comprehensive homing endonuclease target site specificity profiling reveals evolutionary constraints and enables genome engineering applications. Nucleic Acids Res., 40, 2587-2598.
59. Miller, J. C., Tan, S., Qiao, G., Barlow, K. A., Wang, J., Xia, D. F., Meng, X., Paschon, D. E., Leung, E., Hinkley, S. J. et al. (2011) A TALE nuclease architecture for efficient genome editing. Nat. Biotechnol., 29, 143-148.
60. Li, T., Huang, S., Zhao, X., Wright, D. A., Carpenter, S., Spalding, M. H., Weeks, D. P. and Yang, B. (2011) Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res., 39, 6315-6325.
61. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E. and Church, G. M. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823-826.
62. Cradick, T. J., Fine, E. J., Antico, C. J. and Bao, G. (2013) CRISPR/Cas9 systems targeting β-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res, 41, 9584-9592.
63. Hsu, P. D., Scott, D. A., Weinstein, J. A., Ran, F. A., Konermann, S., Agarwala, V., Li, Y., Fine, E. J., Wu, X., Shalem, O. et al. (2013) DNA targeting specificity of RNA-guided Cas9 nucleases. Nat. Biotechnol., 31, 827-832.
64. Esvelt, K. M., Mali, P., Braff, J. L., Moosburner, M., Yaung, S. J. and Church, G. M. (2013) Orthogonal Cas9 proteins for RNA-guided gene regulation and editing. Nat. Methods, 10, 1116-1121.
65. Jinek, M., Jiang, F., Taylor, D. W., Sternberg, S. H., Kaya, E., Ma, E., Anders, C., Hauer, M., Zhou, K., Lin, S. et al. (2014) Structures of Cas9 Endonucleases Reveal RNA-Mediated Conformational Activation. Science, 343, 1247997.
66. Nishimasu, H., Ran, F. A., Hsu, P. D., Konermann, S., Shehata, S. I., Dohmae, N., Ishitani, R., Zhang, F. and Nureki, O. (2014) Crystal structure of Cas9 in complex with Guide RNA and target DNA. Cell, 156, 935-949.