The Structural Basis of Asymmetry in DNA Binding and Cleavage as Exhibited by the I-SmaMI LAGLIDADG Meganuclease

Journal of Molecular Biology

Volumn 428, Issue 1, 2016, Pages 206-220

  Shen, Betty W ^a   Lambert, Abigail ^a   Walker, Bradley C ^b   Stoddard, Barry L ^a   Kaiser, Brett K ^b  

^a Fred Hutchinson Cancer Research Center   (United States)

^b SEATTLE UNIVERSITY   (United States)

Author keywords

genome editing; homing endonuclease; nickase; protein DNA interactions; surface potential

Indexed keywords

CYTOCHROME C OXIDASE; DEOXYRIBONUCLEASE; DOUBLE STRANDED DNA; LYSINE; MEGANUCLEASE; UNCLASSIFIED DRUG; DNA; ENDONUCLEASE;

ARTICLE; BASE PAIRING; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DNA BINDING; DNA CLEAVAGE; DNA CLEAVAGE ASSAY; DNA SEQUENCE; DNA STRAND; ENZYME ACTIVE SITE; ENZYME STRUCTURE; FLOW CYTOMETRY; GENE TARGETING; HINGE REGION; NONHUMAN; NUCLEOPHILICITY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; SORDARIA MACROSPORA; SORDARIALES; STOP CODON; CHEMISTRY; DNA MUTATIONAL ANALYSIS; GENETICS; HYDROLYSIS; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA; DNA MUTATIONAL ANALYSIS; ENDONUCLEASES; HYDROLYSIS; MODELS, MOLECULAR; POINT MUTATION; PROTEIN CONFORMATION;

EID: 84961329116     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2015.12.005     Document Type: Article

References (54)

1. D.J. Segal, and J.F. Meckler Genome engineering at the dawn of the golden age Annu. Rev. Genomics Hum. Genet. 14 2013 135 158
2. A. Dupuy, J. Valton, S. Leduc, J. Armier, R. Galetto, A. Gouble, C. Lebuhotel, A. Stary, F. Paques, P. Duchateau, and et al. Targeted gene therapy of xeroderma pigmentosum cells using meganuclease and TALEN PLoS One 8 2013 e78678
3. L. Popplewell, T. Koo, X. Leclerc, A. Duclert, K. Mamchaoui, A. Gouble, V. Mouly, T. Voit, F. Paques, F. Cedrone, and et al. Gene correction of a Duchenne muscular dystrophy mutation by meganuclease-enhanced exon knock-in Hum. Gene Ther. 24 2013 692 701
4. S. Grosse, N. Huot, C. Mahiet, S. Arnould, S. Barradeau, D.L. Clerre, I. Chion-Sotinel, C. Jacqmarcq, B. Chapellier, A. Ergani, and et al. Meganuclease-mediated inhibition of HSV1 infection in cultured cells Mol. Ther. 19 2011 694 702
5. J.T. Schiffer, M. Aubert, N.D. Weber, E. Mintzer, D. Stone, and K.R. Jerome Targeted DNA mutagenesis for the cure of chronic viral infections J. Virol. 86 2012 8920 8936
6. P. Tebas, D. Stein, W.W. Tang, I. Frank, S.Q. Wang, G. Lee, S.K. Spratt, R.T. Surosky, M.A. Giedlin, G. Nichol, and et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV N. Engl. J. Med. 370 2014 901 910
7. A.E. Ricroch, and M.C. Henard-Damave Next biotech plants: New traits, crops, developers and technologies for addressing global challenges Crit. Rev. Biotechnol. 2015 10.3109/07388551.2015.1004521 [Epub ahead of print]
8. S. Byrne, P. Mali, and G.M. Church Genome editing in human stem cells Methods Enzymol. 546 2014 119 138
9. K. Chiba, and D. Hockemeyer Genome editing in human pluripotent stem cells using site-specific nucleases Methods Mol. Biol. 1239 2015 267 280
10. S. Menoret, S. Fontaniere, D. Jantz, L. Tesson, R. Thinard, S. Remy, C. Usal, L.H. Ouisse, A. Fraichard, and I. Anegon Generation of Rag1-knockout immunodeficient rats and mice using engineered meganucleases FASEB J. 27 2013 703 711
11. Y.S. Chan, R. Takeuchi, J. Jarjour, D.S. Huen, B.L. Stoddard, and S. Russell The design and in vivo evaluation of engineered I-OnuI-based enzymes for HEG gene drive PLoS One 8 2013 e74254
12. R. Galizi, L.A. Doyle, M. Menichelli, F. Bernardini, A. Deredec, A. Burt, B.L. Stoddard, N. Windbichler, and A. Crisanti A synthetic sex ratio distortion system for the control of the human malaria mosquito Nat. Commun. 5 2014 3977
13. K. Pauwels, N. Podevin, D. Breyer, D. Carroll, and P. Herman Engineering nucleases for gene targeting: Safety and regulatory considerations New Biotechnol. 31 2014 18 27
14. S. Boissel, J. Jarjour, A. Astrakhan, A. Adey, A. Gouble, P. Duchateau, J. Shendure, B.L. Stoddard, M.T. Certo, D. Baker, and et al. megaTALs: A rare-cleaving nuclease architecture for therapeutic genome engineering Nucleic Acids Res. 42 2014 2591 2601
15. J.P. Guilinger, D.B. Thompson, and D.R. Liu Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification Nat. Biotechnol. 32 2014 577 582
16. S.Q. Tsai, N. Wyvekens, C. Khayter, J.A. Foden, V. Thapar, D. Reyon, M.J. Goodwin, M.J. Aryee, and J.K. Joung Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing Nat. Biotechnol. 32 2014 569 576
17. B.D. Sather, G.S. Romano Ibarra, K. Sommer, G. Curinga, M. Hale, I.F. Khan, S. Singh, Y. Song, K. Gwiazda, J. Sahni, and et al. Efficient modification of CCR5 in primary human hematopoietic cells using a megaTAL nuclease and AAV donor template Sci. Transl. Med. 2015 10.1126/scitranslmed.aac5530
18. B.L. Stoddard Homing endonucleases from mobile group I introns: Discovery to genome engineering Mob. DNA 5 2014 1 15
19. J.H. Eastberg, A. McConnell Smith, L. Zhao, J. Ashworth, B.W. Shen, and B.L. Stoddard Thermodynamics of DNA target site recognition by homing endonucleases Nucleic Acids Res. 35 2007 7209 7221
20. A. Perrin, M. Buckle, and B. Dujon Asymmetrical recognition and activity of the I-SceI endonuclease on its site and on intron-exon junctions EMBO J. 12 1993 2939 2947
21. S.B. Thyme, J. Jarjour, R. Takeuchi, J.J. Havranek, J. Ashworth, A.M. Scharenberg, B.L. Stoddard, and D. Baker Exploitation of binding energy for catalysis and design Nature 461 2009 1300 1304
22. S.B. Thyme, S.J. Boissel, S. Arshiya Quadri, T. Nolan, D.A. Baker, R.U. Park, L. Kusak, J. Ashworth, and D. Baker Reprogramming homing endonuclease specificity through computational design and directed evolution Nucleic Acids Res. 42 2014 2564 2576
23. R. Takeuchi, A. Lambert, A. Mak, K. Jacoby, R. Dickson, G. Gloor, A. Scharenberg, D. Edgell, and B. Stoddard Tapping natural reservoirs of homing endonucleases for targeted gene modification Proc. Natl. Acad. Sci. U. S. A. 108 2011 13077 13082
24. R.J. Roberts, M. Belfort, T. Bestor, A.S. Bhagwat, T.A. Bickle, J. Bitinaite, R.M. Blumenthal, S. Degtyarev, D.T. Dryden, K. Dybvig, and et al. A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes Nucleic Acids Res. 31 2003 1805 1812
25. S.K. Baxter, A.R. Lambert, A.M. Scharenberg, and J. Jarjour Flow cytometric assays for interrogating LAGLIDADG homing endonuclease DNA-binding and cleavage properties Methods Mol. Biol. 978 2013 45 61
26. S.K. Baxter, A.M. Scharenberg, and A.R. Lambert Engineering and flow-cytometric analysis of chimeric LAGLIDADG homing endonucleases from homologous I-OnuI-family enzymes Methods Mol. Biol. 1123 2014 191 221
27. M.S. Jurica, R.J. Monnat Jr., and B.L. Stoddard DNA recognition and cleavage by the LAGLIDADG homing endonuclease I- CreI Mol. Cell 2 1998 469 476
28. J.M. Bolduc, P.C. Spiegel, P. Chatterjee, K.L. Brady, M.E. Downing, M.G. Caprara, R.B. Waring, and B.L. Stoddard Structural and biochemical analyses of DNA and RNA binding by a bifunctional homing endonuclease and group I intron splicing factor Genes Dev. 17 2003 2875 2888
29. G.H. Silva, and M. Belfort Analysis of the LAGLIDADG interface of the monomeric homing endonuclease I-DmoI Nucleic Acids Res. 32 2004 3156 3168
30. B. Chevalier, M. Turmel, C. Lemieux, R.J. Monnat, and B.L. Stoddard Flexible DNA target site recognition by divergent homing endonuclease isoschizomers I-CreI and I-MsoI J. Mol. Biol. 329 2003 253 269
31. C.M. Moure, F.S. Gimble, and F.A. Quiocho The crystal structure of the gene targeting homing endonuclease I-SceI reveals the origins of its target site specificity J. Mol. Biol. 334 2003 685 696
32. A. McConnell Smith, R. Takeuchi, S. Pellenz, L. Davis, N. Maizels, R.J. Monnat Jr., and B.L. Stoddard 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 2009 5099 5104
33. R. Molina, M.J. Marcaida, P. Redondo, M. Marenchino, P. Duchateau, M. D'Abramo, G. Montoya, and J. Prieto Engineering a nickase on the homing endonuclease I-DmoI scaffold J. Biol. Chem. 290 2015 18534 18544
34. Y. Niu, K. Tenney, H. Li, and F.S. Gimble Engineering variants of the I-SceI homing endonuclease with strand-specific and site-specific DNA-nicking activity J. Mol. Biol. 382 2008 188 202
35. T.J. Dolinsky, P. Czodrowski, H. Li, J.E. Nielsen, J.H. Jensen, G. Klebe, and N.A. Baker PDB2PQR: Expanding and upgrading automated preparation of biomolecular structures for molecular simulations Nucleic Acids Res. 35 2007 W522 W525
36. N.A. Baker, D. Sept, S. Joseph, M.J. Holst, and J.A. McCammon Electrostatics of nanosystems: Application to microtubules and the ribosome Proc. Natl. Acad. Sci. U. S. A. 98 2001 10037 10041
37. R. Joshi, K.K. Ho, K. Tenney, J.H. Chen, B.L. Golden, and F.S. Gimble Evolution of I-SceI homing endonucleases with increased DNA recognition site specificity J. Mol. Biol. 405 2011 185 200
38. H. Li, S. Pellenz, U. Ulge, B.L. Stoddard, and R.J. Monnat Jr. Generation of single-chain LAGLIDADG homing endonucleases from native homodimeric precursor proteins Nucleic Acids Res. 37 2009 1650 1662
39. J. Prieto, P. Redondo, D. Padro, S. Arnould, J.C. Epinat, F. Paques, F.J. Blanco, and G. Montoya The C-terminal loop of the homing endonuclease I-CreI is essential for site recognition, DNA binding and cleavage Nucleic Acids Res. 35 2007 3262 3271
40. M.J. Marcaida, J. Prieto, P. Redondo, A.D. Nadra, A. Alibes, L. Serrano, S. Grizot, P. Duchateau, F. Paques, F.J. Blanco, and et al. 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 2008 16888 16893
41. S.E. Halford, and J.F. Marko How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res. 32 2004 3040 3052
42. P.H. von Hippel, and O.G. Berg On the specificity of DNA-protein interactions Proc. Natl. Acad. Sci. U. S. A. 83 1986 1608 1612
43. C.W. Garvie, and C. Wolberger Recognition of specific DNA sequences Mol. Cell 8 2001 937 946
44. N.M. Luscombe, R.A. Laskowski, and J.M. Thornton Amino acid-base interactions: A three-dimensional analysis of protein-DNA interactions at an atomic level Nucleic Acids Res. 29 2001 2860 2874
45. C.G. Kalodimos, N. Biris, A.M. Bonvin, M.M. Levandoski, M. Guennuegues, R. Boelens, and R. Kaptein Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes Science 305 2004 386 389
46. R.S. Spolar, and M.T. Record Jr. Coupling of local folding to site-specific binding of proteins to DNA Science 263 1994 777 784
47. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode C.W. Carter Jr. R.M. Sweet, Methods in Enzymology 276 1997 Academic Press New York, NY 307 326
48. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674
49. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr. D Biol. Crystallogr. 66 2010 486 501
50. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr. D Biol. Crystallogr. 53 1997 240 255
51. W. DeLano The PyMOL Molecular Graphics System Version 1.7.4 Schrödinger, LLC 2004
52. N. Jullien, and J.P. Herman LUEGO: A cost and time saving gel shift procedure BioTechniques 51 2011 267 269
53. K.J. Minch, T.R. Rustad, E.J. Peterson, J. Winkler, D.J. Reiss, S. Ma, M. Hickey, W. Brabant, B. Morrison, S. Turkarslan, and et al. The DNA-binding network of Mycobacterium tuberculosis Nat. Commun. 6 2015 5829
54. M. Scalley-Kim, A. McConnell-Smith, and B.L. Stoddard Coevolution of homing endonuclease specificity and its host target sequence J. Mol. Biol. 372 2007 1305 1319