Structural basis of asymmetric DNA methylation and ATP-triggered long-range diffusion by EcoP15I

Nature Communications

Volumn 6, Issue , 2015, Pages

  Gupta, Yogesh K ^a   Chan, Siu Hong ^b   Xu, Shuang Yong ^b   Aggarwal, Aneel K ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEW ENGLAND BIOLABS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; ECOP151 ENZYME; HOLOENZYME; PROTEIN; RECA1 PROTEIN; RECA2 PROTEIN; UNCLASSIFIED DRUG; DNA; DNA HELICASE; DNA MODIFICATION METHYLASE ECOP15I; SITE SPECIFIC DNA METHYLTRANSFERASE (ADENINE SPECIFIC);

DIFFUSION; DNA; ENZYME ACTIVITY; HYDROLYSIS; METABOLISM;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DIFFUSION; DNA CONFORMATION; DNA METABOLISM; DNA METHYLATION; DNA STRAND; ENZYME ACTIVITY; ENZYME STRUCTURE; HYDROLYSIS; INTERACTIONS WITH DNA; MAMMAL CELL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RNA METABOLISM; RNA METHYLATION; STRUCTURE ANALYSIS; CHEMISTRY; CRYSTALLIZATION; ESCHERICHIA COLI; METABOLISM; MOLECULAR DOCKING; X RAY CRYSTALLOGRAPHY;

MAMMALIA;

ADENOSINE TRIPHOSPHATE; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DIFFUSION; DNA; DNA HELICASES; DNA METHYLATION; ESCHERICHIA COLI; HYDROLYSIS; MOLECULAR DOCKING SIMULATION; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC);

EID: 84931281606     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8363     Document Type: Article

References (65)

1. Haberman, A. The bacteriophage P1 restriction endonuclease. J. Mol. Biol. 89, 545-563 (1974).
2. Haberman, A., Heywood, J. & Meselson, M. DNA modification methylase activity of Escherichia coli restriction endonucleases K and P. Proc. Natl Acad. Sci. USA 69, 3138-3141 (1972).
3. Meselson, M. & Yuan, R. DNA restriction enzyme from E. coli. Nature 217, 1110-1114 (1968).
4. Arber, W. & Wauters-Willems, D. Host specificity of DNA produced by Escherichia coli. XII. The two restriction and modification systems of strain 15T. Mol. Gen. Genet. 108, 203-217 (1970).
5. Roberts, R. J., Vincze, T., Posfai, J. & Macelis, D. REBASE-a database for DNA restriction and modification: Enzymes, genes and genomes. Nucleic Acids Res. 43, D298-D299 (2015).
6. Raghavendra, N. K., Bheemanaik, S. & Rao, D. N. Mechanistic insights into type III restriction enzymes. Front. Biosci. (Landmark Ed.) 17, 1094-1107 (2012).
7. Gupta, Y. K. et al. Structural insights into the assembly and shape of Type III restriction-modification (R-M) EcoP15I complex by small-angle X-ray scattering. J. Mol. Biol. 420, 261-268 (2012).
8. Janscak, P., Sandmeier, U., Szczelkun, M. D. & Bickle, T. A. Subunit assembly and mode of DNA cleavage of the type III restriction endonucleases EcoP1I and EcoP15I. J. Mol. Biol. 306, 417-431 (2001).
9. Wyszomirski, K. H. et al. Type III restriction endonuclease EcoP15I is a heterotrimeric complex containing one Res subunit with several DNA-binding regions and ATPase activity. Nucleic Acids Res. 40, 3610-3622 (2012).
10. Butterer, A. et al. Type III restriction endonucleases are heterotrimeric: Comprising one helicase-nuclease subunit and a dimeric methyltransferase that binds only one specific DNA. Nucleic Acids Res. 42, 5139-5150 (2014).
11. Meisel, A., Bickle, T. A., Kruger, D. H. & Schroeder, C. Type III restriction enzymes need two inversely oriented recognition sites for DNA cleavage. Nature 355, 467-469 (1992).
12. Van Aelst, K. et al. Type III restriction enzymes cleave DNA by long-range interaction between sites in both head-to-head and tail-to-tail inverted repeat. Proc. Natl Acad. Sci. USA 107, 9123-9128 (2010).
13. Gorbalenya, A. E. & Koonin, E. V. Endonuclease (R) subunits of type-I and type-III restriction-modification enzymes contain a helicase-like domain. FEBS Lett. 291, 277-281 (1991).
14. Singleton, M. R., Dillingham, M. S. & Wigley, D. B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76, 23-50 (2007).
15. Reiser, J. & Yuan, R. Purification and properties of the P15 specific restriction endonuclease from Escherichia coli. J. Biol. Chem. 252, 451-456 (1977).
16. Ramanathan, S. P. et al. Type III restriction enzymes communicate in 1D without looping between their target sites. Proc. Natl Acad. Sci. USA 106, 1748-1753 (2009).
17. Meisel, A., Mackeldanz, P., Bickle, T. A., Kruger, D. H. & Schroeder, C. Type III restriction endonucleases translocate DNA in a reaction driven by recognition site-specific ATP hydrolysis. EMBO J. 14, 2958-2966 (1995).
18. Crampton, N. et al. DNA looping and translocation provide an optimal cleavage mechanism for the type III restriction enzymes. EMBO J. 26, 3815-3825 (2007).
19. Schwarz, F. W. et al. The helicase-like domains of type III restriction enzymes trigger long-range diffusion along DNA. Science 340, 353-356 (2013).
20. Blainey, P. C. et al. Nonspecifically bound proteins spin while diffusing along DNA. Nat. Struct. Mol. Biol. 16, 1224-1229 (2009).
21. Szczelkun, M. D. Roles for helicases as ATP-dependent molecular switches. Adv. Exp. Med. Biol. 767, 225-244 (2013).
22. Qiu, R. et al. Large conformational changes in MutS during DNA scanning, mismatch recognition and repair signalling. EMBO J. 31, 2528-2540 (2012).
23. Gorman, J. et al. Single-molecule imaging reveals target-search mechanisms during DNA mismatch repair. Proc. Natl Acad. Sci. USA 109, E3074-E3083 (2012).
24. Cho, W. K. et al. ATP alters the diffusion mechanics of MutS on mismatched DNA. Structure 20, 1264-1274 (2012).
25. Ahmad, I., Krishnamurthy, V. & Rao, D. N. DNA recognition by the EcoP15I and EcoPI modification methyltransferases. Gene 157, 143-147 (1995).
26. Klimasauskas, S., Kumar, S., Roberts, R. J. & Cheng, X. HhaI methyltransferase flips its target base out of the DNA helix. Cell 76, 357-369 (1994).
27. Goedecke, K., Pignot, M., Goody, R. S., Scheidig, A. J. & Weinhold, E. Structure of the N6-adenine DNA methyltransferase M.TaqI in complex with DNA and a cofactor analog. Nat. Struct. Biol. 8, 121-125 (2001).
28. Zhong, X. et al. Molecular mechanism of action of plant DRM De novo DNA methyltransferases. Cell 157, 1050-1060 (2014).
29. Jia, D., Jurkowska, R. Z., Zhang, X., Jeltsch, A. & Cheng, X. Structure of Dnmt3a bound to Dnmt3L suggests a model for De novo DNA methylation. Nature 449, 248-251 (2007).
30. Meyer, K. D. & Jaffrey, S. R. The dynamic epitranscriptome: N6-methyladenosine and gene expression control. Nat. Rev. Mol. Cell Biol. 15, 313-326 (2014).
31. Stunnenberg, H. G., Vermeulen, M. & Atlasi, Y. Developmental biology. A Me6Age for pluripotency. Science 347, 614-615 (2015).
32. Rao, D. N., Dryden, D. T. & Bheemanaik, S. Type III restriction-modification enzymes: A historical perspective. Nucleic Acids Res. 42, 45-55 (2013).
33. Durr, H., Korner, C., Muller, M., Hickmann, V. & Hopfner, K. P. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 121, 363-373 (2005).
34. Malone, T., Blumenthal, R. M. & Cheng, X. Structure-guided analysis reveals nine sequence motifs conserved among DNA amino-methyltransferases, and suggests a catalytic mechanism for these enzymes. J. Mol. Biol. 253, 618-632 (1995).
35. Schneider, B., Neidle, S. & Berman, H. M. Conformations of the sugarphosphate backbone in helical DNA crystal structures. Biopolymers 42, 113-124 (1997).
36. Lukacs, C. M., Kucera, R., Schildkraut, I. & Aggarwal, A. K. Understanding the immutability of restriction enzymes: Crystal structure of BglII and its DNA substrate at 1.5A resolution [see comments]. Nat. Struct. Biol. 7, 134-140 (2000).
37. Sengoku, T., Nureki, O., Nakamura, A., Kobayashi, S. & Yokoyama, S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125, 287-300 (2006).
38. Thoma, N. H. et al. Structure of the SWI2/SNF2 chromatin-remodeling domain of eukaryotic Rad54. Nat. Struct. Mol. Biol. 12, 350-356 (2005).
39. Kim, J. L. et al. Hepatitis C virus NS3 RNA helicase domain with a bound oligonucleotide: The crystal structure provides insights into the mode of unwinding. Structure 6, 89-100 (1998).
40. Morgan, R. D., Dwinell, E. A., Bhatia, T. K., Lang, E. M. & Luyten, Y. A. The MmeI family: Type II restriction-modification enzymes that employ single-strand modification for host protection. Nucleic Acids Res. 37, 5208-5221 (2009).
41. Shen, B. W. et al. Characterization and crystal structure of the type IIG restriction endonuclease RM.BpuSI. Nucleic Acids Res. 39, 8223-8236 (2011).
42. Scavetta, R. D. et al. Structure of RsrI methyltransferase, a member of the N6-adenine beta class of DNA methyltransferases. Nucleic Acids Res. 28, 3950-3961 (2000).
43. Osipiuk, J., Walsh, M. A. & Joachimiak, A. Crystal structure of MboIIA methyltransferase. Nucleic Acids Res. 31, 5440-5448 (2003).
44. Thomas, C. B. & Gumport, R. I. Dimerization of the bacterial RsrI N6-adenine DNA methyltransferase. Nucleic Acids Res. 34, 806-815 (2006).
45. Meyer, K. D. et al. Comprehensive analysis of mRNA methylation reveals enrichment in 3' UTRs and near stop codons. Cell 149, 1635-1646 (2012).
46. Dominissini, D. et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485, 201-206 (2012).
47. Batista, P. J. et al. m(6)A RNA modification controls cell fate transition in mammalian embryonic stem cells. Cell Stem Cell 15, 707-719 (2014).
48. Geula, S. et al. m6A mRNA methylation facilitates resolution of naive pluripotency toward differentiation. Science 347, 1002-1006 (2015).
49. Wang, Y. et al. N6-methyladenosine modification destabilizes developmental regulators in embryonic stem cells. Nat. Cell Biol. 16, 191-198 (2014).
50. Ping, X. L. et al. Mammalian WTAP is a regulatory subunit of the RNA N6-methyladenosine methyltransferase. Cell Res. 24, 177-189 (2014).
51. Liu, J. et al. A METTL3-METTL14 complex mediates mammalian nuclear RNA N6-adenosine methylation. Nat. Chem. Biol. 10, 93-95 (2014).
52. Bujnicki, J. M., Feder, M., Radlinska, M. & Blumenthal, R. M. Structure prediction and phylogenetic analysis of a functionally diverse family of proteins homologous to the MT-A70 subunit of the human mRNA:m(6)A methyltransferase. J. Mol. Evol. 55, 431-444 (2002).
53. Michel, G. et al. The structure of the RlmB 23 S rRNA methyltransferase reveals a new methyltransferase fold with a unique knot. Structure 10, 1303-1315 (2002).
54. Thomas, S. R., Keller, C. A., Szyk, A., Cannon, J. R. & Laronde-Leblanc, N. A. Structural insights into the functional mechanism of Nep1/Emg1 N1-specific pseudouridine methyltransferase in ribosome biogenesis. Nucleic Acids Res. 39, 2445-2457 (2011).
55. Schubert, H. L., Blumenthal, R. M. & Cheng, X. Many paths to methyltransfer: A chronicle of convergence. Trends Biochem Sci. 28, 329-335 (2003).
56. Gorbalenya, A. E. & Koonin, E. V. Helicases: Amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3, 419-429 (1993).
57. Kelch, B. A., Makino, D. L., O'Donnell, M. & Kuriyan, J. How a DNA polymerase clamp loader opens a sliding clamp. Science 334, 1675-1680 (2011).
58. Skoglund, C. M., Smith, H. O. & Chandrasegaran, S. Construction of an efficient overproducer clone of HinfI restriction endonuclease using the polymerase chain reaction. Gene 88, 1-5 (1990).
59. Fortelle, d. L. & Bricogne, G. Maximum-likelihood heavy atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494 (1997).
60. Hendrickson, W. A. Determination of macromolecular structures from anomalous diffraction of synchrotron radiation. Science 254, 51-58 (1991).
61. Vonrhein, C. et al. Data processing and analysis with the autoPROC toolbox. Acta Crystallogr. D Biol. Crystallogr. 67, 293-302 (2011).
62. Emsley, P. & Cowtan, K. Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
63. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr. 60, 2210-2221 (2004).
64. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
65. McCoy, A. J., Grosse-Kunstleve, R. W., Storoni, L. C. & Read, R. J. Likelihoodenhanced fast translation functions. Acta Crystallogr. D Biol. Crystallogr. 61, 458-464 (2005).