A unified genetic, computational and experimental framework identifies functionally relevant residues of the homing endonuclease I-BmoI

Nucleic Acids Research

Volumn 38, Issue 7, 2010, Pages 2411-2427

  Kleinstiver, Benjamin P ^a   Fernandes, Andrew D ^a   Gloor, Gregory B ^a,b   Edgell, David R ^a  

^a WESTERN UNIVERSITY   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARAGINE; ENDONUCLEASE; PROLINE; TYROSINE; AMINO ACID; DEOXYRIBONUCLEASE; I BMOI ENDONUCLEASE; I-BMOI ENDONUCLEASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BIOINFORMATICS; CALCULATION; COMPUTER ANALYSIS; GENETIC ANALYSIS; INFORMATION PROCESSING; INFORMATION RETRIEVAL; PHENOTYPE; PREDICTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; STRUCTURE ANALYSIS; BIOLOGY; CHEMICAL STRUCTURE; CHEMISTRY; DNA CLEAVAGE; ENZYME ACTIVE SITE; GENETICS; METABOLISM; METHODOLOGY; MOLECULAR EVOLUTION; MUTATION; PROTEIN TERTIARY STRUCTURE; STATISTICAL ANALYSIS;

AMINO ACIDS; CATALYTIC DOMAIN; COMPUTATIONAL BIOLOGY; DATA INTERPRETATION, STATISTICAL; DNA CLEAVAGE; ENDODEOXYRIBONUCLEASES; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

EID: 77952316381     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp1223     Document Type: Article

References (50)

1. Capra, J.A. and Singh, M. (2007) Predicting functionally important residues from sequence conservation. Bioinformatics, 23, 1875-1882.
2. Landau, M., Mayrose, I., Rosenberg, Y., Glaser, F., Martz, E., Pupko, T. and Ben-Tal, N. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res., 33, W299-W302.
3. Watson, J.D., Laskowski, R.A. and Thornton, J.M. (2005) Predicting protein function from sequence and structural data. Curr. Opin. Struct. Biol., 15, 275-284.
4. Martin, L.C., Gloor, G.B., Dunn, S.D. and Wahl, L.M. (2005) Using information theory to search for co-evolving residues in proteins. Bioinformatics, 21, 4116-4124.
5. Tillier, E.R. and Lui, T.W. (2003) Using multiple interdependency to separate functional from phylogenetic correlations in protein alignments. Bioinformatics, 19, 750-755.
6. Stoddard, B.L. (2005) Homing endonuclease structure and function. Q. Rev. Biophys., 38, 49-95.
7. Belfort, M., Derbyshire, V., Cousineau, B. and Lambowitz, A. (2002) In Craig, N., Craigie, R., Gellert, M. and Lambowitz, A. (eds), Mobile DNA II. ASM Press, New York, pp. 761-783.
8. Zhao, L., Bonocora, R.P., Shub, D.A. and Stoddard, B.L. (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.
9. Dassa, B., London, N., Stoddard, B.L., Schueler-Furman, O. and 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.
10. Grizot, S., Smith, J., Daboussi, F., Prieto, J., Redondo, P., Merino, N., Villate, M., Thomas, S., Lemaire, L., Montoya, G. et al. (2009) Efficient targeting of a SCID gene by an engineered single-chain homing endonuclease. Nucleic Acids Res., 37, 5405-5419.
11. Rosen, L.E., Morrison, H.A., Masri, S., Brown, M.J., Springstubb, B., Sussman, D., Stoddard, B.L. and Seligman, L.M. (2006) Homing endonuclease I-CreI derivatives with novel DNA target specificities. Nucleic Acids Res., 34, 4791-4800.
12. Ashworth, J., Havranek, J.J., Duarte, C.M., Sussman, D., Monnat, R.J. Jr, Stoddard, B.L. and Baker, D. (2006) Computational redesign of endonuclease DNA binding and cleavage specificity. Nature, 441, 656-659.
13. 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.
14. Quirk, S.M., Bell-Pedersen, D. and 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.
15. Derbyshire, V., Kowalski, J.C., Dansereau, J.T., Hauer, C.R. and Belfort, M. (1997) Two-domain structure of the td intron-encoded endonuclease I-TevI correlates with the two-domain configuration of the homing site. J. Mol. Biol., 265, 494-506.
16. Bell-Pedersen, D., Quirk, S.M., Bryk, M. and 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.
17. Liu, Q., Dansereau, J.T., Puttamadappa, S.S., Shekhtman, A., Derbyshire, V. and 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.
18. Liu, Q., Derbyshire, V., Belfort, M. and Edgell, D.R. (2006) Distance determination by GIY-YIG intron endonucleases: discrimination between repression and cleavage functions. Nucleic Acids Res., 34, 1755-1764.
19. Dean, A.B., Stanger, M.J., Dansereau, J.T., Van Roey, P., Derbyshire, V. and Belfort, M. (2002) Zinc finger as distance determinant in the flexible linker of intron endonuclease I-TevI. Proc. Natl Acad. Sci. USA, 99, 8554-8561.
20. Kowalski, J.C., Belfort, M., Stapleton, M.A., Holpert, M., Dansereau, J.T., Pietrokovski, S., Baxter, S.M. and Derbyshire, V. (1999) Configuration of the catalytic GIY-YIG domain of intron endonuclease I-TevI: coincidence of computational and molecular findings. Nucleic Acids Res., 27, 2115-2125.
21. Truglio, J.J., Rhau, B., Croteau, D.L., Wang, L., Skorvaga, M., Karakas, E., Dellavecchia, M.J., Wang, H., Van Houten, B. and Kisker, C. (2005) Structural insights into the first incision reaction during nucleotide excision repair. EMBO J., 24, 885-894.
22. Lagerback, P. and Carlson, K. (2008) Amino acid residues in the GIY-YIG endonuclease II of phage T4 affecting sequence recognition and binding as well as catalysis. J. Bacteriol., 190, 5533-5544.
23. Dunin-Horkawicz, S., Feder, M. and Bujnicki, J.M. (2006) Phylogenomic analysis of the GIY-YIG nuclease superfamily. BMC Genomics, 7, 98.
24. Pyatkov, K.I., Arkhipova, I.R., Malkova, N.V., Finnegan, D.J. and Evgen'ev, M.B. (2004) Reverse transcriptase and endonuclease activities encoded by Penelope-like retroelements. Proc. Natl Acad. Sci. USA, 101, 14719-14724.
25. Van Roey, P., Meehan, L., Kowalski, J.C., Belfort, M. and Derbyshire, V. (2002) Catalytic domain structure and hypothesis for function of GIY-YIG intron endonuclease I-TevI. Nat. Struct. Biol., 9, 806-811.
26. Ibryashkina, E.M., Zakharova, M.V., Baskunov, V.B., Bogdanova, E.S., Nagornykh, M.O., Den'mukhamedov, M.M., Melnik, B.S., Kolinski, A., Gront, D., Feder, M. et al. (2007) Type II restriction endonuclease R.Eco29kI is a member of the GIY-YIG nuclease superfamily. BMC Struct. Biol., 7, 48.
27. Carter, J.M., Friedrich, N.C., Kleinstiver, B. and Edgell, D.R. (2007) Strand-specific contacts and divalent metal ion regulate double-strand break formation by the GIY-YIG homing endonuclease I-BmoI. J. Mol. Biol., 374, 306-321.
28. Van Roey, P. and Derbyshire, V. (2005) In Belfort, M.S.B., Wood, D.W. and Derbyshire, V. (eds), Homing Endonucleases and Inteins. Springer-Verlag, Berlin, pp. 67-83.
29. Mueller, J.E., Smith, D., Bryk, M. and 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.
30. Gasiunas, G., Sasnauskas, G., Tamulaitis, G., Urbanke, C., Razaniene, D. and Siksnys, V. (2008) Tetrameric restriction enzymes: expansion to the GIY-YIG nuclease family. Nucleic Acids Res., 36, 938-949.
31. Ibryashkina, E.M., Sasnauskas, G., Solonin, A.S., Zakharova, M.V. and Siksnys, V. (2009) Oligomeric structure diversity within the GIY-YIG nuclease family. J. Mol. Biol., 387, 10-16.
32. Edgell, D.R. and Shub, D.A. (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.
33. Edgell, D.R., Stanger, M.J. and Belfort, M. (2003) Importance of a single base pair for discrimination between intron-containing and intronless alleles by endonuclease I-BmoI. Curr. Biol., 13, 973-978.
34. Chen, Z. and Zhao, H. (2005) A highly sensitive selection method for directed evolution of homing endonucleases. Nucleic Acids Res., 33, e154.
35. Waterhouse, A.M., Procter, J.B., Martin, D.M., Clamp, M. and Barton, G.J. (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics, 25, 1189-1191.
36. Eswar, N., Marti-Renom, A., Webb, B., Madhusudhan, M.S., Eramian, D., Shen, M., Pieper, U. and Sali, A. (2006) Comparative protein structure modeling with MODELLER. Curr. Prot. Bioinform., 15, 5.6.1-5.6.30.
37. Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics, 22, 195-201.
38. Dunn, S.D., Wahl, L.M. and Gloor, G.B. (2008) Mutual information without the influence of phylogeny or entropy dramatically improves residue contact prediction. Bioinformatics, 24, 333-340.
39. Wu, W., Wood, D.W., Belfort, G., Derbyshire, V. and Belfort, M. (2002) Intein-mediated purification of cytotoxic endonuclease I-TevI by insertional inactivation and pH-controllable splicing. Nucleic Acids Res., 30, 4864-4871.
40. Deminoff, S.J., Tornow, J. and Santangelo, G.M. (1995) Unigenic evolution: a novel genetic method localizes a putative leucine zipper that mediates dimerization of the Saccharomyces cerevisiae regulator Gcr1p. Genetics, 141, 1263-1274.
41. Behrsin, C.D., Brandl, C.J., Litchfield, D.W., Shilton, B.H. and Wahl, L.M. (2006) Development of an unbiased statistical method for the analysis of unigenic evolution. BMC Bioinformatics, 7, 150.
42. Flick, K.E., Jurica, M.S., Monnat, R.J. Jr and Stoddard, B.L. (1998) DNA binding and cleavage by the nuclear intron-encoded homing endonuclease I-PpoI. Nature, 394, 96-101.
43. Galburt, E.A., Chadsey, M.S., Jurica, M.S., Chevalier, B.S., Erho, D., Tang, W., Monnat, R.J. Jr and Stoddard, B.L. (2000) Conformational changes and cleavage by the homing endonuclease I-PpoI: a critical role for a leucine residue in the active site. J. Mol. Biol., 300, 877-887.
44. Bryk, M., Belisle, M., Mueller, J.E. and Belfort, M. (1995) Selection of a remote cleavage site by I-TevI, the td intron-encoded endonuclease. J. Mol. Biol., 247, 197-210.
45. Sitbon, E. and Pietrokovski, S. (2003) New types of conserved sequence domains in DNA-binding regions of homing endonucleases. Trends Biochem. Sci., 28, 473-477.
46. Van Roey, P., Waddling, C.A., Fox, K.M., Belfort, M. and Derbyshire, V. (2001) Intertwined structure of the DNA-binding domain of intron endonuclease I-TevI with its substrate. EMBO J., 20, 3631-3637.
47. Shen, B.W., Landthaler, M., Shub, D.A. and Stoddard, B.L. (2004) DNA binding and cleavage by the HNH homing endonuclease I-HmuI. J. Mol. Biol., 342, 43-56.
48. Behrsin, C.D., Bailey, M.L., Bateman, K.S., Hamilton, K.S., Wahl, L.M., Brandl, C.J., Shilton, B.H. and Litchfield, D.W. (2007) Functionally important residues in the peptidyl-prolyl isomerase Pin1 revealed by unigenic evolution. J. Mol. Biol., 365, 1143-1162.
49. Zeng, X., Zhang, D., Dorsey, M. and Ma, J. (2003) Hypomutable regions of yeast TFIIB in a unigenic evolution test represent structural domains. Gene, 309, 49-56.
50. Schneider, T.D. and Stephens, R.M. (1990) Sequence logos: a new way to display consensus sequences. Nucleic Acids Res., 18, 6097-6100.