A molecular dynamics study of slow base flipping in DNA using conformational flooding

Biophysical Journal

Volumn 93, Issue 3, 2007, Pages 770-786

  Bouvier, Benjamin ^a   Grubmüller, Helmut ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DNA BASE; DNA FRAGMENT; GUANOSINE;

ARTICLE; BASE PAIRING; DNA CONFORMATION; DNA HELIX; DNA REPLICATION; DNA TRANSCRIPTION; ENERGY; ENERGY TRANSFER; MATHEMATICAL ANALYSIS; MOLECULAR DYNAMICS; MOLECULAR GENETICS; SIMULATION; TECHNIQUE;

EID: 34547819823     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.091751     Document Type: Article

References (63)

1. 237 for active flipping of its target cytosine. Structure. 12:1047-1055.
2. Klimasauskas, S., S. Kumar, R. J. Roberts, and X. D. Cheng. 1994. Hhal methyltransferase flips its target base out of the DNA helix. Cell. 76:357-369.
3. Klimasauskas, S., and R. J. Roberts. 1995. Disruption of the target G-C base-pair by the HhaI methyltransferase. Gene. 157:163-164.
4. Klimasauskas, S., T. Szyperski, S. Serva, and K. Wuthrich. 1998. Dynamic modes of the flipped-out cytosine during HhaI methyltransferase-DNA interactions in solution. EMBO J. 17:317-324.
5. Slupphaug, G., C. D. Mol, B. Kavli, A. S. Arvai, H. E. Krokan, and J. A. Tainer. 1996. A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature. 384:87-92.
6. Stivers, J. T., K. W. Pankiewicz, and K. A. Watanabe. 1999. Kinetic mechanism of damage site recognition and uracil flipping by Escherichia coli uracil DNA glycosylase. Biochemistry. 38:952-963.
7. Luo, J., and T. C. Bruice. 2005. Low-frequency normal mode in DNA HhaI methyltransferase and motions of residues involved in the base flipping. Proc. Natl. Acad. Sci. USA. 102:16194-16198.
8. O'Gara, M., J. R. Horton, R. J. Roberts, and X. D. Cheng. 1998. Structures of Hhal methyltransferase complexed with substrates containing mismatches at the target base. Nat. Struct. Biol. 5:872-877.
9. Parikh, S. S., G. Walcher, G. D. Jones, G. Slupphaug, H. E. Krokan, G. M. Blackburn, and J. A. Tainer. 2000. Uracil-DNA glycosylase-DNA substrate and product structures: conformational strain promotes catalytic efficiency by coupled stereoelectronic effects. Proc. Natl. Acad. Sci. USA. 97:5083-5088.
10. Huang, N., N. K. Banavali, and A. D. MacKerell. 2003. Protein-facilitated base flipping in DNA by cytosine-5-methyltransferase. Proc. Natl. Acad. Sci. USA. 100:68-73.
11. Gueron, M., and J. L. Leroy. 1995. Studies of basepair kinetics by NMR measurement of proton exchange. In Nuclear Magnetic Resonance And Nucleic Acids. Academic Press, San Diego, CA.
12. Leijon, M., and A. Graslund. 1992. Effects of sequence and length on imino proton-exchange and basepair opening kinetics in DNA oligonucleotide duplexes. Nucleic Acids Res. 20:5339-5343.
13. Leroy, J. L., M. Kochoyan, T. Huynhdinh, and M. Gueron. 1988. Characterization of base-pair opening in deoxynucleotide duplexes using catalyzed exchange of the imino proton. J. Mol. Biol. 200:223-238.
14. Snoussi, K., and J. L. Leroy. 2001. Imino proton exchange and base-pair kinetics in RNA duplexes. Biochemistry. 40:8898-8904.
15. Neely, R. K., D. Daujotyte, S. Grazulis, S. W. Magennis, D. T. F. Dryden, S. Klimasauskas, and A. C. Jones. 2005. Time-resolved fluorescence of 2-aminopurine as a probe of base flipping in M.HhaI-DNA complexes. Nucleic Acids Res. 33:6953-6960.
16. O'Neil, L. L., and O. Wiest. 2005. A selective, noncovalent assay for base flipping in DNA. J. Am. Chem. Soc. 127:16800-16801.
17. Lyakhov, I. G., P. N. Hengen, D. Rubens, and T. D. Schneider. 2001. The P1 phage replication protein RepA contacts an otherwise inaccessible thymine N3 proton by DNA distortion or base flipping. Nucleic Acids Res. 29:4892-4900.
18. Schneider, T. D. 2001. Strong minor groove base conservation in sequence logos implies DNA distortion or base flipping during replication and transcription initiation. Nucleic Acids Res. 29:4881-4891.
19. Sommer, N., R. Depping, M. Piotrowski, and W. Ruger. 2004. Bacteriophage T4 α-glucosyltransferase: a novel interaction with gp45 and aspects of the catalytic mechanism. Biochem. Biophys. Res. Commun. 323:809-815.
20. Fuxreiter, M., M. Luo, P. Jedlovszky, I. Simon, and R. Osman. 2002. Role of base flipping in specific recognition of damaged DNA by repair enzymes. J. Mol. Biol. 323:823-834.
21. Hopkins, B. B., and N. O. Reich. 2004. Simultaneous DNA binding, bending, and base flipping - evidence for a novel M. EcoRI methyltransferase-DNA complex. J. Biol. Chem. 279:37049-37060.
22. Ramstein, J., and R. Lavery. 1988. Energetic coupling between DNA bending and basepair opening. Proc. Natl. Acad. Sci. USA. 85:7231-7235.
23. Stivers, J. T. 2004. Site-specific DNA damage recognition by enzyme-induced base flipping. In Progress in Nucleic Acid Research and Molecular Biology, Vol 77. Academic Press, San Diego, CA.
24. Keepers, J. W., P. A. Kollman, P. K. Weiner, and T. L. James. 1982. Molecular mechanical studies of DNA flexibility - coupled backbone torsion angles and base-pair openings. Proc. Natl. Acad. Sci. USA. 79:5537-5541.
25. Malta, E., G. F. Moolenaar, and N. Goosen. 2006. Base flipping in nucleotide excision repair. J. Biol. Chem. 281:2184-2194.
26. MacDonald, D., G. Demarre, M. Bouvier, D. Mazel, and D. N. Gopaul. 2006. Structural basis for broad DNA-specificity in integron recombination. Nature. 440:1157-1162.
27. Horton, J. R., G. Ratner, N. K. Banavali, N. Huang, Y. Choi, M. A. Maier, V. E. Marquez, A. D. MacKerell, and X. D. Cheng. 2004. Caught in the act: visualization of an intermediate in the DNA base flipping pathway induced by Hhal methyltransferase. Nucleic Acids Res. 32:3877-3886.
28. Torrie, G. M., and J. P. Valleau. 1977. Non-physical sampling distributions in Monte Carlo free energy estimation - umbrella sampling. J. Comput. Phys. 23:187-199.
29. Kumar, S., D. Bouzida, R. H. Swendsen, P. A. Kollman, and J. M. Rosenberg. 1992. The weighted histogram analysis method for free-energy calculations on biomolecules. 1. The method. J. Comput. Chem. 13:1011-1021.
30. Kumar, S., J. M. Rosenberg, D. Bouzida, R. H. Swendsen, and P. A. Kollman. 1995. Multidimensional free-energy calculations using the weighted histogram analysis method. J. Comput. Chem. 16:1339-1350.
31. Bernet, J., K. Zakrzewska, and R. Lavery. 1997. Modeling basepair opening: the role of helical twist. Theochem. J. Mol. Struct. 398:473-482.
32. Giudice, E., and R. Lavery. 2003. Nucleic acid basepair dynamics: the impact of sequence and structure using free-energy calculations. J. Am. Chem. Soc. 125:4998-4999.
33. Giudice, E., P. Varnai, and R. Lavery. 2003. Basepair opening within B-DNA: free energy pathways for GC and AT pairs from umbrella sampling simulations. Nucleic Acids Res. 31:1434-1443.
34. Giudice, E., P. Varnai, and R. Lavery. 2003. Basepair opening within B-DNA: free energy pathways for GC and AT pairs from umbrella sampling simulations. Nucleic Acids Res. 31:2703.
35. Giudice, E., P. Varnai, and R. Lavery. 2001. Energetic and conformational aspects of A·T base-pair opening within the DNA double helix. ChemPhysChem. 2:673-677.
36. Ramstein, J., and R. Lavery. 1990. Basepair opening pathways in B-DNA. J. Biomol. Struct. Dyn. 7:915-933.
37. Banavali, N. K., and A. D. MacKerell. 2002. Free energy and structural pathways of base flipping in a DNA GCGC containing sequence. J. Mol. Biol. 319:141-160.
38. Huang, N., and A. D. MacKerell. 2005. Specificity in protein-DNA interactions: energetic recognition by the (cytosine-C5)-methyltransferase from HhaI. J. Mol. Biol. 345:265-274.
39. MacKerell, A. D. 2003. Computational studies of base flipping in DNA alone and bound to the cytosine-5-methyltransferase from Hhal. Abstr. Papers Am. Chem. Soc. 226:U431-U431.
40. Priyakumar, U. D., and A. D. MacKerell. 2006. Base flipping in a GCGC containing DNA dodecamer: a comparative study of the performance of the nucleic acid force fields, CHARMM, AMBER, and BMS. J. Chem. Theor. Comput. 2:187-200.
41. Priyakumar, U. D., and A. D. MacKerell. 2006. Computational approaches for investigating base flipping in oligonucleotides. Chem. Rev. 106:489-505.
42. Grubmuller, H. 1995. Predicting slow structural transitions in macromolecular systems - conformational flooding. Phys. Rev. E. 52:2893-2906.
43. Schulze, B. G., H. Grubmuller, and J. D. Evanseck. 2000. Functional significance of hierarchical tiers in carbonmonoxy myoglobin: conformational substates and transitions studied by conformational flooding simulations. J. Am. Chem. Soc. 122:8700-8711.
44. Muller, E. M., A. de Meijere, and H. Grubmuller. 2002. Predicting unimolecular chemical reactions: chemical flooding. J. Chem. Phys. 116:897-905.
45. Diekmann, S. 1989. Definitions and nomenclature of nucleic-acid structure parameters. J. Mol. Biol. 205:787-791.
46. Wang, J. M., P. Cieplak, and P. A. Kollman. 2000. How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J. Comput. Chem. 21:1049-1074.
47. Berendsen, H. J. C., D. Vanderspoel, and R. Vandrunen. 1995. GROMACS - a message-passing parallel molecular-dynamics implementation. Comput. Phys. Commun. 91:43-56.
48. Lindahl, E., B. Hess, and D. van der Spoel. 2001. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Model. (Online). 7:306-317.
49. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald - an N.Log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089-10092.
50. Berendsen, H. J. C., J. P. M. Postma, W. F. Van Gunsteren, A. Dinola, and J. R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690.
51. Hess, B., H. Bekker, H. J. C. Berendsen, and J. Fraaije. 1997. LINCS: a linear constraint solver for molecular simulations. J. Comput. Chem. 18:1463-1472.
52. Macke, T. J., and D. A. Case. 1998. Modeling unusual nucleic acid structures. In Molecular Modeling Of Nucleic Acids, ACS Symposium Series. 379-393.
53. Lavery, R., and H. Sklenar. 1989. Defining the structure of irregular nucleic acids - conventions and principles. J. Biomol. Struct. Dyn. 6:655-667.
54. Nailor, W., and B. Chapman. WNLIB. http://www.willnaylor.com/wnlib.html
55. Press, W. H., B. P. Flannery, S. A. Teukolsky, and W. T. Vetterling. 1988. Numerical Recipes in C. Cambridge University Press, New York.
56. Horton, J. R., X. Zhang, R. Maunus, Z. Yang, G. G. Wilson, R. J. Roberts, and X. D. Cheng. 2006. DNA nicking by HinP1I endonuclease: bending, base flipping and minor groove expansion. Nucleic Acids Res. 34:939-948.
57. Dornberger, U., M. Leijon, and H. Fritzsche. 1999. High basepair opening rates in tracts of GC basepairs. J. Biol. Chem. 274:6957-6962.
58. Chen, Y. Z., V. Mohan, and R. H. Griffey. 1998. Effect of backbone ζ-torsion angle on low energy single base opening in B-DNA crystal structures. Chem. Phys. Lett. 287:570-574.
59. Chen, Y. Z., V. Mohan, and R. H. Griffey. 1998. The opening of a single base without perturbations of neighboring nucleotides: a study on crystal B-DNA duplex d(CGCGAATTCGCG)(2). J. Biomol. Struct. Dyn. 15:765-777.
60. Su, T. J., M. R. Tock, S. U. Egelhaaf, W. C. K. Poon, and D. T. F. Dryden. 2005. DNA bending by M.EcoKI methyltransferase is coupled to nucleotide flipping. Nucleic Acids Res. 33:3235-3244.
61. Nakano, S., Y. Uotani, K. Uenishi, M. Fujii, and N. Sugimoto. 2005. DNA base flipping by a basepair-mimic nucleoside. Nucleic Acids Res. 33:7111-7119.
62. Laio, A., and M. Parrinello. 2002. Escaping free-energy minima. Proc. Natl. Acad. Sci. USA. 99:12562-12566.
63. Fukunishi, Y., Y. Mikami, and H. Nakamura. 2003. The filling potential method: a method for estimating the free energy surface for protein-ligand docking. J. Phys. Chem. B. 107:13201-13210.