A structural basis for the preferential binding of hemimethylated DNA by HhaI DNA methyltransferase

Journal of Molecular Biology

Volumn 263, Issue 4, 1996, Pages 597-606

  O'Gara, Margaret ^a   Roberts, Richard J ^b   Cheng, Xiaodong ^a  

^a W M Keck Structural Biology Laboratory   (United States)

^b NEW ENGLAND BIOLABS   (United States)

Author keywords

5 methyl 2' deoxycytidine; DNA base flipping; Hemimethylated DNA; Long range electrostatic interactions; Van der Waals' interactions

Indexed keywords

5 METHYLDEOXYCYTIDINE; COMPLEMENTARY DNA; CYTOSINE; DEOXYCYTIDINE; DNA METHYLTRANSFERASE; DOUBLE STRANDED DNA; GLUTAMIC ACID;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA HELIX; DNA METHYLATION; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN DNA BINDING; STEREOCHEMISTRY;

EID: 0030575782     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0601     Document Type: Article

References (33)

1. Anderson, J. E., Ptashne, M. & Harrison, S. C. (1987). Structure of the repressor-operator complex of bacteriophage 434. Nature, 326, 846-852.
2. Bestor, T. H. & Ingram, V. M. (1983). Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA. Proc. Natl Acad. Sci. USA, 80, 5559-5563.
3. Bestor, T., Laudano, A., Mattaliano, R. & Ingram, V. (1988). Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases. J. Mol. Biol. 203, 971-983.
4. Bolden, A. H., Nalin, C. M., Ward, C. A., Poonian, M. S. & Weissbach, A. (1986). Primary DNA sequence determines sites of maintenance and de novo methylation by mammalian DNA methyltransferases. Mol. Cell. Biol. 6, 1135-1140.
5. Brunger, A. T. (1992). X-PLOR: A System for X-ray Crystallography and NMR. Version 3.1. New Haven, Connecticut. Yale University Press.
6. Chen, L., MacMillan, A. M. & Verdine, G. L. (1993). Mutational separation of DNA binding from catalysis in a DNA cytosine methyltransferase. J. Am. Chem. Soc. 115, 5318-5319.
7. Cheng, X. & Blumenthal, R. M. (1996). Finding a basis for flipping bases. Structure, 4, 639-645.
8. Cheng, X., Kumar, S., Klimašauskas, S. & Roberts, R. J. (1993). Crystal structure of the HhaI DNA methyltransferase. Cold Spring Harbor Symp. Quant. Biol. 58, 331-338.
9. Clark, K. L., Halay, E. D., Lai, E. & Burley, S. K. (1993). Co-crystal structure of the HNF-3/fork head DNA recognition motif resembles histone H5. Nature, 364, 412-420.
10. Collaborative Computing Project, Number 4. (1994). The CCP4 suite: programs for protein crystallography. Acta Crystallog. Sect. D, 50, 760-763.
11. Dubey, A. K. & Roberts, R. J. (1992). Sequence-specific DNA binding by the MspI DNA methyltransferase. Nucl. Acids Res. 20, 3167-3173.
12. Ellenberger, T. E., Brandi, C. S., Struhl, K. & Harrison, S. C. (1992). The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted α helix: crystal structure of the protein-DNA complex. Cell, 71, 1223-1237.
13. Furey, W. & Swaminathan, S. (1996). PHASES-a program package for the processing and analysis of diffraction data from macromolecules. Methods Enzymol. In the press.
14. Gruenbaum, Y., Cedar, H. & Razin, A. (1982). Substrate and sequence specificity of a eukaryotic DNA methylase. Nature, 295, 620-622.
15. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. Sect. A, 47, 110-119.
16. Kelleher, J. E., Daniel, A. S. & Murray, N. E. (1991). Mutations that confer de novo activity upon a maintenance methyltransferase. J. Mol. Biol. 221, 431-440.
17. Klimašauskas, S., Kumar, S. Roberts, R. J. & Cheng. X. (1994). HhaI methyltransferase flips its target base out of the DNA helix. Cell, 76, 357-369.
18. Kraulis, P. J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.
19. Kumar, S., Cheng, X., Pflugrath, J. W. & Roberts, R. J. (1992). Purification, crystallization, and preliminary X-ray diffraction analysis of an M.HteI-AdoMet complex. Biochemistry, 31, 8648-8653.
20. Lauster, R., Trautner, T. A. & Noyer-Weidner, M. (1989). Cytosine-specific type II DNA methyltransferases. A conserved enzyme core with variable target-recognizing domains. J. Mol. Biol. 206, 305-312.
21. Nicholls, A., Sharp, K. A. & Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11, 281-296.
22. O'Gara, M., Klimasauskas, S., Roberts, R. J. & Cheng, X. (1996). Enzymatic C5-cytosine methylation of DNA: mechanistic implications of new crystal structures for HhaI methyltransferase-DNA-AdoHcy complexes. J. Mol. Biol. 261, 634-645.
23. Phillips, K. & Phillips, S. E. V. (1994). Electrostatic activation of Escherichia coli methionine repressor. Structure, 2, 309-316.
24. Reich, N. O. & Mashhoon, N. (1990). Inhibition of EcoRI DNA methylase with cofactor analogs. J. Biol. Chem. 265, 8966-8970.
25. Reinisch, K. M., Chen, L., Verdine, G. L. & Lipscomb, W. N. (1994). Crystallization and preliminary crystallographic analysis of a DNA (cytosine-5)-methyltransferase from Haemophilus aegypthis bound covalently to DNA. J. Mol. Biol. 238, 626-629.
26. Reinisch, K. M., Chen. L., Verdine, G. L. & Lipscomb, W. N. (1995). The crystal structure of HaeIII methyltransferase covalently complexed to DNA: an extrahelical cytosine and rearranged base-pairing. Cell, 82, 143-153.
27. Schluckebier, G., Labahn, J., Granzin, J., Schildkraut, I. & Saenger, W. (1995). A model for DNA binding and enzyme action derived from crystallographic studies of the TaqI N6-adenine-methyltransferase. Gene, 157, 131-134.
28. Smith, S. S., Kan, J. L. C., Baker, D. J., Kaplan, B. E. & Dembek, P. (1991). Recognition of unusual DNA structures by human DNA(cytosine-5)methyltransferase. J. Mol. Biol. 217, 39-51.
29. Suck, D., Lahm, A. & Oefner, C. (1988). Structure refined to 2 Å of a nicked DNA octanucleotide complex with DNase I. Nature, 332, 464-468.
30. Suri, B., Nagaraja, V. & Bickle, T. A. (1984). Bacterial DNA modification. Curr. Topics Microbiol. Immunol. 108, 1-9.
31. Suzuki, M. (1994). A framework for the DNA-protein recognition code of the probe helix in transcription factors: the chemical and stereochemical rules. Structure, 2, 317-326.
32. Szczelkun, M. D. & Connolly, B. A. (1995). Sequence-specific binding of DNA by the EcoRV restriction and modification enzymes with nucleic acid and cofactor analogues. Biochemistry, 34, 10724-10733.
33. Taylor, I., Watts D. & Kneale, G. (1993). Substrate recognition and selectivity in the type IC DNA modification methylase M.EcoR124I. Nucl. Acids Res. 21, 4929-4935.