Distal structural elements coordinate a conserved base flipping network

Biochemistry

Volumn 52, Issue 10, 2013, Pages 1669-1676

  Matje, Douglas M ^a   Krivacic, Cody T ^a   Dahlquist, Frederick W ^a   Reich, Norbert O ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASE FLIPPING; DNA MODIFICATION; EXPERIMENTAL TECHNIQUES; METHYLTRANSFERASES; REPAIR ENZYMES; SPECIFIC CONTACT; STRUCTURAL ELEMENTS; SUBSTRATE RECOGNITION;

COMPLEX NETWORKS; DNA; ENZYMES; REPAIR;

AMINO ACIDS;

ALANINE; AMINO ACID; GLYCINE; SERINE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; DNA HELIX; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME STRUCTURE; ENZYME SUBSTRATE; MUTATION; PRIORITY JOURNAL;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CONSERVED SEQUENCE; DNA; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA-CYTOSINE METHYLASES; HAEMOPHILUS; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84874979495     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301284f     Document Type: Article

References (39)

1. Estabrook, R. A., Luo, J., Purdy, M. M., Sharma, V., Weakliem, P., Bruice, T. C., and Reich, N. O. (2005) Statistical coevolution analysis and molecular dynamics: Identification of amino acid pairs essential for catalysis Proc. Natl. Acad. Sci. U.S.A. 102, 994-999
2. Luo, J. and Bruice, T. C. (2005) Low-frequency normal mode in DNA HhaI methyltransferase and motions of residues involved in the base flipping Proc. Natl. Acad. Sci. U.S.A. 102, 16194-16198
3. Boehr, D. D., Nussinov, R., and Wright, P. E. (2009) The role of dynamic conformational ensembles in biomolecular recognition Nat. Chem. Biol. 5, 789-796
4. Bhabha, G., Lee, J., Ekiert, D. C., Gam, J., Wilson, I. A., Dyson, H. J., Benkovic, S. J., and Wright, P. E. (2011) A dynamic knockout reveals that conformational fluctuations influence the chemical step of enzyme catalysis Science 332, 234-238
5. Cheng, X., Kumar, S., Posfai, J., Pflugrath, J. W., and Roberts, R. J. (1993) Crystal structure of the HhaI DNA methyltransferase complexed with S-adenosyl- l -methionine Cell 74, 299-307
6. Klimasauskas, S., Kumar, S., Roberts, R. J., and Cheng, X. (1994) Hhal methyltransferase flips its target base out of the DNA helix Cell 76, 357-369
7. Daujotyt, S., Vilkaitis, S., Merkien, G., Venclovas, C., and Klimasauskas, S. (2004) HhaI DNA Methyltransferase Uses the Protruding Gln237 for Active Flipping of Its Target Cytosine Structure 12, 1047-1055
8. Horton, J. R., Ratner, G., Banavali, N. K., Huang, N., Choi, Y., Maier, M. A., Marquez, V. E., MacKerell, A. D., Jr., and Cheng, X. (2004) Caught in the act: Visualization of an intermediate in the DNA base-flipping pathway induced by HhaI methyltransferase Nucleic Acids Res. 32, 3877-3886
9. Huang, N. and MacKerell, A. D., Jr. (2005) Specificity in protein-DNA interactions: Energetic recognition by the (cytosine-C5)-methyltransferase from HhaI J. Mol. Biol. 345, 265-274
10. Shieh, F.-K., Youngblood, B., and Reich, N. O. (2006) The role of Arg165 towards base flipping, base stabilization and catalysis in M.HhaI J. Mol. Biol. 362, 516-527
11. Huang, N. and MacKerell, A. D., Jr. (2004) Atomistic view of base flipping in DNA Philos. Trans. R. Soc., A 362, 1439-1460
12. Gerasimaite, R., Merkiene, E., and Klimasauskas, S. (2011) Direct observation of cytosine flipping and covalent catalysis in a DNA methyltransferase Nucleic Acids Res. 39, 3771-3780
13. Matje, D. M., Coughlin, D. F., Connolly, B. A., Dahlquist, F. W., and Reich, N. O. (2011) Determinants of precatalytic conformational transitions in the DNA cytosine methyltransferase M.HhaI Biochemistry 50, 1465-1473
14. Estabrook, R. A. and Reich, N. (2006) Observing an Induced-fit Mechanism during Sequence-specific DNA Methylation J. Biol. Chem. 281, 37205-37214
15. Cavaluzzi, M. J. and Borer, P. N. (2004) Revised UV extinction coefficients for nucleoside-5′-monophosphates and unpaired DNA and RNA Nucleic Acids Res. 32, e13
16. Youngblood, B., Buller, F., and Reich, N. O. (2006) Determinants of sequence-specific DNA methylation: Target recognition and catalysis are coupled in M.HhaI Biochemistry 45, 15563-15572
17. Coman, D. and Russu, I. M. (2005) A nuclear magnetic resonance investigation of the energetics of basepair opening pathways in DNA Biophys. J. 89, 3285-3292
18. O'Gara, M., Klimasauskas, S., Roberts, R. J., and 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
19. Huang, N. and MacKerell, A. D., Jr. (2004) Atomistic View of Base Flipping in DNA Philos. Trans. R. Soc., A 362, 1439-1460
20. Huang, N., Banavali, N. K., and MacKerell, A. D., Jr. (2003) Protein-facilitated base flipping in DNA by cytosine-5-methyltransferase Proc. Natl. Acad. Sci. U.S.A. 100, 68-73
21. Merkiene, E. and Klimasauskas, S. (2005) Probing a rate-limiting step by mutational perturbation of AdoMet binding in the HhaI methyltransferase Nucleic Acids Res. 33, 307-315
22. Estabrook, R. A., Nguyen, T. T., Fera, N., and Reich, N. O. (2009) Coupling sequence-specific recognition to DNA modification J. Biol. Chem. 284 (34) 22690-22696
23. Matje, D. M. and Reich, N. O. (2012) Molecular drivers of base flipping during sequence-specific DNA methylation ChemBioChem 13 (11) 1574-1577
24. Klimasauskas, S., Szyperski, T., Serva, S., and Wuthrich, K. (1998) Dynamic modes of the flipped-out cytosine during HhaI methyltransferase-DNA interactions in solution EMBO J. 17, 317-324
25. Malygin, E. G., Evdokimov, A. A., Zinoviev, V. V., Ovechkina, L. G., Lindstrom, W. M., Reich, N. O., Schlagman, S. L., and Hattman, S. (2001) A dual role for substrate S-adenosyl- l -methionine in the methylation reaction with bacteriophage T4 Dam DNA-[N6-adenine]-methyltransferase Nucleic Acids Res. 29, 2361-2369
26. Parker, J. B., Bianchet, M. A., Krosky, D. J., Friedman, J. I., Amzel, L. M., and Stivers, J. T. (2007) Enzymatic capture of an extrahelical thymine in the search for uracil in DNA Nature 449, 433-437
27. Jiang, Y. L. and Stivers, J. T. (2002) Mutational analysis of the base-flipping mechanism of uracil DNA glycosylase Biochemistry 41, 11236-11247
28. Cao, C., Jiang, Y. L., Krosky, D. J., and Stivers, J. T. (2006) The catalytic power of uracil DNA glycosylase in the opening of thymine base pairs J. Am. Chem. Soc. 128 (40) 13034-13035
29. Wong, I., Lundquist, A. J., Bernards, A. S., and Mosbaugh, D. W. (2002) Presteady-state analysis of a single catalytic turnover by Escherichia coli uracil-DNA glycosylase reveals a "pinch-pull-push" mechanism J. Biol. Chem. 277, 19424-19432
30. Vilkaitis, G., Dong, A., Weinhold, E., Cheng, X., and Klimašauskas, S. (2000) Functional Roles of the Conserved Threonine 250 in the Target Recognition Domain of HhaI DNA Methyltransferase J. Biol. Chem. 275, 38722-38730
31. Reinisch, K. M., Chen, L., Verdine, G. L., and Lipscomb, W. N. (1995) The crystal structure of HaeIII methyltransferase convalently complexed to DNA: An extrahelical cytosine and rearranged base pairing Cell 82, 143-153
32. Jia, D., Jurkowska, R. Z., Zhang, X., Jeltsch, A., and Cheng, X. (2007) Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation Nature 449, 248-251
33. Song, J., Rechkoblit, O., Bestor, T. H., and Patel, D. J. (2011) Structure of DNMT1-DNA complex reveals a role for autoinhibition in maintenance DNA methylation Science 331, 1036-1040
34. Takeshita, K., Suetake, I., Yamashita, E., Suga, M., Narita, H., Nakagawa, A., and Tajima, S. (2011) Structural insight into maintenance methylation by mouse DNA methyltransferase 1 (Dnmt1) Proc. Natl. Acad. Sci. U.S.A. 108, 9055-9059
35. Kempf, J. G., Jung, J. Y., Ragain, C., Sampson, N. S., and Loria, J. P. (2007) Dynamic requirements for a functional protein hinge J. Mol. Biol. 368, 131-149
36. Jin, Z. and Johnson, K. A. (2011) Role of a GAG hinge in the nucleotide-induced conformational change governing nucleotide specificity by T7 DNA polymerase J. Biol. Chem. 286, 1312-1322
37. Bouvignies, G., Vallurupalli, P., Hansen, D. F., Correia, B. E., Lange, O., Bah, A., Vernon, R. M., Dahlquist, F. W., Baker, D., and Kay, L. E. (2011) Solution structure of a minor and transiently formed state of a T4 lysozyme mutant Nature 477, 111-114
38. Youngblood, B., Shieh, F. K., De Los Rios, S., Perona, J. J., and Reich, N. O. (2006) Engineered extrahelical base destabilization enhances sequence discrimination of DNA methyltransferase M.HhaI J. Mol. Biol. 362, 334-346
39. Holz-Schietinger, C., Matje, D. M., Flexer-Harrison, M., and Reich, N. O. (2011) Oligomerization of DNMT3A controls the mechanism of de novo DNA methylation J. Biol. Chem. 286 (48) 41479-41488