The recognition domain of the methyl-specific endonuclease McrBC flips out 5-methylcytosine

Nucleic Acids Research

Volumn 40, Issue 15, 2012, Pages 7552-7562

  Sukackaite, Rasa ^a,b   Grazulis, Saulius ^a   Tamulaitis, Gintautas ^a   Siksnys, Virginijus ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; ENDONUCLEASE; PROTEIN MCRB N; PROTEIN MCRBC; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA BINDING MOTIF; DNA METHYLATION; DNA MODIFICATION; DNA PROTEIN COMPLEX; ENZYME STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL;

5-METHYLCYTOSINE; AMINO ACID SEQUENCE; BINDING SITES; DNA; DNA RESTRICTION ENZYMES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION DOMAINS AND MOTIFS;

EID: 84867319588     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks332     Document Type: Article

References (61)

1. Bird, A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev., 16, 6-21.
2. Tost, J. (2010) DNA methylation: an introduction to the biology and the disease-associated changes of a promising biomarker. Mol. Biotechnol., 44, 71-81.
3. Henderson, I. R. and Jacobsen, S. E. (2007) Epigenetic inheritance in plants. Nature, 447, 418-424.
4. Ho, K. L., McNae, I. W., Schmiedeberg, L., Klose, R. J., Bird, A. P. and Walkinshaw, M. D. (2008) MeCP2 binding to DNA depends upon hydration at methyl-CpG. Mol. Cell, 29, 525-531.
5. Arita, K., Ariyoshi, M., Tochio, H., Nakamura, Y. and Shirakawa, M. (2008) Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature, 455, 818-821.
6. Avvakumov, G. V., Walker, J. R., Xue, S., Li, Y., Duan, S., Bronner, C., Arrowsmith, C. H. and Dhe-Paganon, S. (2008) Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature, 455, 822-825.
7. Hashimoto, H., Horton, J. R., Zhang, X., Bostick, M., Jacobsen, S. E. and Cheng, X. (2008) The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature, 455, 826-829.
8. Rajakumara, E., Law, J. A., Simanshu, D. K., Voigt, P., Johnson, L. M., Reinberg, D., Patel, D. J. and Jacobsen, S. E. (2011) A dual flip-out mechanism for 5mC recognition by the Arabidopsis SUVH5 SRA domain and its impact on DNA methylation and H3K9 dimethylation in vivo. Genes Dev., 25, 137-152.
9. Iyer, L. M., Abhiman, S. and Aravind, L. (2011) Natural history of eukaryotic DNA methylation systems. Prog. Mol. Biol. Transl. Sci., 101, 25-104.
10. Bickle, T. A. and Kruger, D. H. (1993) Biology of DNA restriction. Microbiol. Rev., 57, 434-450.
11. Ishikawa, K., Fukuda, E. and Kobayashi, I. (2010) Conflicts targeting epigenetic systems and their resolution by cell death: novel concepts for methyl-specific and other restriction systems. DNA Res., 17, 325-342.
12. Warren, R. A. (1980) Modified bases in bacteriophage DNAs. Annu. Rev. Microbiol., 34, 137-158.
13. Hattman, S. and Fukasawa, T. (1963) Host-induced modification of T-even phages due to defective glucosylation of their DNA. Proc. Natl Acad. Sci. USA, 50, 297-300.
14. Shedlovsky, A. and Brenner, S. (1963) A chemical basis for the host-induced modification of T-even bacteriophages. Proc. Natl Acad. Sci. USA, 50, 300-305.
15. Raleigh, E. A., Trimarchi, R. and Revel, H. (1989) Genetic and physical mapping of the mcrA (rglA) and mcrB (rglB) loci of Escherichia coli K-12. Genetics, 122, 279-296.
16. Luria, S. E. and Human, M. L. (1952) A nonhereditary, host-induced variation of bacterial viruses. J. Bacteriol., 64, 557-569.
17. Hiom, K. and Sedgwick, S. G. (1991) Cloning and structural characterization of the mcrA locus of Escherichia coli. J. Bacteriol., 173, 7368-7373.
18. Sutherland, E., Coe, L. and Raleigh, E. A. (1992) McrBC: a multisubunit GTP-dependent restriction endonuclease. J. Mol. Biol., 225, 327-348.
19. Roberts, R. J., Vincze, T., Posfai, J. and Macelis, D. (2010) REBASE-a database for DNA Restriction and modification: enzymes, genes and genomes. Nucleic Acids Res., 38, D234-D236.
20. Kruger, T., Wild, C. and Noyer-Weidner, M. (1995) McrB: a prokaryotic protein specifically recognizing DNA containing modified cytosine residues. EMBO J., 14, 2661-2669.
21. Dila, D., Sutherland, E., Moran, L., Slatko, B. and Raleigh, E. A. (1990) Genetic and sequence organization of the mcrBC locus of Escherichia coli K-12. J. Bacteriol., 172, 4888-4900.
22. Pieper, U. and Pingoud, A. (2002) A mutational analysis of the PD. D/EXK motif suggests that McrC harbors the catalytic center for DNA cleavage by the GTP-dependent restriction enzyme McrBC from Escherichia coli. Biochemistry, 41, 5236-5244.
23. Pieper, U., Brinkmann, T., Kruger, T., Noyer-Weidner, M. and Pingoud, A. (1997) Characterization of the interaction between the restriction endonuclease McrBC from E. coli and its cofactor GTP. J. Mol. Biol., 272, 190-199.
24. Neuwald, A. F., Aravind, L., Spouge, J. L. and Koonin, E. V. (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res., 9, 2743.
25. Pieper, U., Schweitzer, T., Groll, D. H., Gast, F. U. and Pingoud, A. (1999) The GTP-binding domain of McrB: more than just a variation on a common theme? J. Mol. Biol., 292, 547-556.
26. White, S. R. and Lauring, B. (2007) AAA+ATPases: achieving diversity of function with conserved machinery. Traffic, 8, 1657-1667.
27. Panne, D., Muller, S. A., Wirtz, S., Engel, A. and Bickle, T. A. (2001) The McrBC restriction endonuclease assembles into a ring structure in the presence of G nucleotides. EMBO J., 20, 3210-3217.
28. Stewart, F. J. and Raleigh, E. A. (1998) Dependence of McrBC cleavage on distance between recognition elements. Biol. Chem., 379, 611-616.
29. Panne, D., Raleigh, E. A. and Bickle, T. A. (1999) The McrBC endonuclease translocates DNA in a reaction dependent on GTP hydrolysis. J. Mol. Biol., 290, 49-60.
30. Gast, F. U., Brinkmann, T., Pieper, U., Kruger, T., Noyer-Weidner, M. and Pingoud, A. (1997) The recognition of methylated DNA by the GTP-dependent restriction endonuclease McrBC resides in the N-terminal domain of McrB. Biol. Chem., 378, 975-982.
31. Stewart, F. J., Panne, D., Bickle, T. A. and Raleigh, E. A. (2000) Methyl-specific DNA binding by McrBC, a modification-dependent restriction enzyme. J. Mol. Biol., 298, 611-622.
32. Pieper, U., Schweitzer, T., Groll, D. H. and Pingoud, A. (1999) Defining the location and function of domains of McrB by deletion mutagenesis. Biol. Chem., 380, 1225-1230.
33. Leslie, A. G. (2006) The integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr., 62, 48-57.
34. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D Biol. Crystallogr., 62, 72-82.
35. French, G. S. and Wilson, K. S. (1978) On the treatment of negative intensity observations. Acta Crystallogr., A34, 517-525.
36. CCP4. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr., 50, 760-763.
37. Sheldrick, G. M. (2008) A short history of SHELX. Acta Crystallogr. A, 64, 112-122.
38. Panjikar, S., Parthasarathy, V., Lamzin, V. S., Weiss, M. S. and Tucker, P. A. (2005) Auto-Rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr. D Biol. Crystallogr., 61, 449-457.
39. Morris, R. J., Perrakis, A. and Lamzin, V. S. (2002) ARP/wARP's model-building algorithms. I. The main chain. Acta Crystallogr. D Biol. Crystallogr., 58, 968-975.
40. Vagin, A. and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr., 66, 22-25.
41. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
42. Brunger, A. T., Adams, P. D., Clore, G. M., De Lano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S. et al. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr., 54, 905-921.
43. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr., 53, 240-255.
44. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B. 3rd, Snoeyink, J., Richardson, J. S. et al. (2007) MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res., 35, W375-W383.
45. Luscombe, N. M., Laskowski, R. A. and Thornton, J. M. (1997) NUCPLOT: a program to generate schematic diagrams of protein-nucleic acid interactions. Nucleic Acids Res., 25, 4940-4945.
46. Lavery, R. and Sklenar, H. (1988) The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J. Biomol. Struct. Dyn., 6, 63-91.
47. Martin, A. M., Sam, M. D., Reich, N. O. and Perona, J. J. (1999) Structural and energetic origins of indirect readout in site-specific DNA cleavage by a restriction endonuclease. Nat. Struct. Biol., 6, 269-277.
48. Combet, C., Blanchet, C., Geourjon, C. and Deleage, G. (2000) NPS@: network protein sequence analysis. Trends Biochem. Sci., 25, 147-150.
49. Berry, D. A., Jung, K., Wise, D. S., Sercel, D. A., Pearson, W. H., Mackie, H., Randolph, J. B. and Somers, R. L. (2004) Pyrrolo-dC and pyrrolo-C: fluorescent analogs of cytidine and 2'-deoxycytidine for the study of oligonucleotides. Tetrahedron Lett., 45, 2457-2461.
50. Liu, C. and Martin, C. T. (2001) Fluorescence characterization of the transcription bubble in elongation complexes of T7 RNA polymerase. J. Mol. Biol., 308, 465-475.
51. Dash, C., Rausch, J. W. and Le Grice, S. F. (2004) Using pyrrolo-deoxycytosine to probe RNA/DNA hybrids containing the human immunodeficiency virus type-1 3' polypurine tract. Nucleic Acids Res., 32, 1539-1547.
52. Tinsley, R. A. and Walter, N. G. (2006) Pyrrolo-C as a fluorescent probe for monitoring RNA secondary structure formation. RNA, 12, 522-529.
53. Holz, B., Klimasauskas, S., Serva, S. and Weinhold, E. (1998) 2-Aminopurine as a fluorescent probe for DNA base flipping by methyltransferases. Nucleic Acids Res., 26, 1076-1083.
54. Tamulaitis, G., Zaremba, M., Szczepanowski, R. H., Bochtler, M. and Siksnys, V. (2007) Nucleotide flipping by restriction enzymes analyzed by 2-aminopurine steady-state fluorescence. Nucleic Acids Res., 35, 4792-4799.
55. Holm, L., Kaariainen, S., Rosenstrom, P. and Schenkel, A. (2008) Searching protein structure databases with DaliLite v. 3. Bioinformatics, 24, 2780-2781.
56. Li, N., Sickmier, E. A., Zhang, R., Joachimiak, A. and White, S. W. (2002) The MotA transcription factor from bacteriophage T4 contains a novel DNA-binding domain: the 'double wing' motif. Mol. Microbiol., 43, 1079-1088.
57. Singarapu, K. K., Liu, G., Xiao, R., Bertonati, C., Honig, B., Montelione, G. T. and Szyperski, T. (2007) NMR structure of protein yjbR from Escherichia coli reveals 'double-wing' DNA binding motif. Proteins, 67, 501-504.
58. Defossez, P. A. and Stancheva, I. (2010) Biological functions of methyl-CpG-binding proteins. Prog. Mol. Biol. Transl. Sci., 101, 377-398.
59. Lau, A. Y., Scharer, O. D., Samson, L., Verdine, G. L. and Ellenberger, T. (1998) Crystal structure of a human alkylbase-DNA repair enzyme complexed to DNA: mechanisms for nucleotide flipping and base excision. Cell, 95, 249-258.
60. Ponferrada-Marin, M. I., Parrilla-Doblas, J. T., Roldan-Arjona, T. and Ariza, R. R. (2011) A discontinuous DNA glycosylase domain in a family of enzymes that excise 5-methylcytosine. Nucleic Acids Res., 39, 1473-1484.
61. Raleigh, E. A. and Wilson, G. (1986) Escherichia coli K-12 restricts DNA containing 5-methylcytosine. Proc. Natl Acad. Sci. USA, 83, 9070-9074.