Atomistic view of base flipping in DNA

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 362, Issue 1820, 2004, Pages 1439-1460

  Huang, Niu ^a   MacKerell Jr , Alexander D ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

Author keywords

Base flipping; DNA repair; Methylation; Molecular dynamics; Potential of mean force; Watson Crick

Indexed keywords

EID: 3042572329     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2004.1383     Document Type: Article

References (70)

1. Banavali, N. K. & MacKerell Jr, A. D. 2002 Free energy and structural pathways of base flipping in a DNA GCGC containing sequence. J. Mol. Biol. 319, 141-160.
2. Banavali, N., Huang, N. & MacKerell, A. D. 2004 Presence of specific backbone conformational patterns during DNA base flipping. (In preparation.)
3. Becker, O. M., MacKerell Jr, A. D., Roux, B. & Watanabe, M. (eds) 2001 Computational biochemistry and biophysics. New York: Marcel Dekker.
4. Beglov, D. & Roux, B. 1994 Finite representation of an infinite bulk system: solvent boundary potential for computer simulations. J. Chem. Phys. 100, 9050-9063.
5. Beglov, D. & Roux, B. 1997 An integral equation to describe the solvation of polar molecules in liquid water. J. Phys. Chem. 101, 7821-7826.
6. + channel. Nature 414, 73-77.
7. Bernet, J., Zakrzewska, K. & Lavery, R. 1997 Modelling base pair opening: the role of helical twist. J. Mol. Struct. 398, 473-482.
8. Beveridge, D. L. & DiCapua, F. M. 1989 Free energy via molecular simulations: applications to chemical and biomolecular systems. A. Rev. Biophys. Biophys. Chem. 18, 431-492.
9. Boresch, S., Archontis, G. & Karplus, G. 1994 Free energy simulations: the meaning of the individual contributions from a component analysis. Proteins 20, 25-33.
10. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S. & Karplus, M. 1983 CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217.
11. Chen, Y.-Z., Mohan, V. & Grifrey, R. H. 2000 Sponteneous base flipping in DNA and its possible role in methyltransferase binding. Phys. Rev. E 62, 1133-1137.
12. Cheng, X. & Blumenthal, R. M. 1996 Finding a basis for flipping bases. Structure 4, 639-645.
13. Cheng, X. & Roberts, R. J. 2001 AdoMet-dependent methylation, DNA methyltransferases and base flipping. Nucleic Acids Res. 29, 3784-3795.
14. Cheng, X., Kumar, S., Posfai, J., Pflugrath, J. W. & Roberts, R. J. 1993 Crystal structure of the HhaI DNA methyltransferase complexed with S-adenosyl-L-methionine. Cell 74, 299-307.
15. Cramer, C. J. 2002 Essentials of computational chemistry theories and models. Wiley.
16. Crouzy, S., Baudry, J., Smith, J. C. & Roux, B. 1999 Efficient calculation of two-dimensional adiabatic and free energy maps: application to the isomerization of the C13=C14 and C15=N16 bonds in the retinal of bacteriorhodopsin. J. Comput. Chem. 20, 1644-1658.
17. Darden, T. A., York, D. & Pedersen, L. G. 1993 Particle mesh Ewald: an N log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092.
18. Dornberger, U., Leijon, M. & Fritzsche, H. 1999 High base pair opening rates in tracts of GC base pairs. J. Biol. Chem. 274, 6954-6962.
19. Foloppe, N. & MacKerell Jr, A. D. 1999 Intrinsic conformational properties of deoxyribonuclecsides: implicated role for cytosine in the equilibrium between the A, B and Z forms of DNA. Biophys. J. 76, 3206-3218.
20. Foloppe, N. & MacKerell Jr, A. D. 2000 All-atom empirical force field for nucleic acids. I. Parameter optimization based on small molecule and condensed phase macromolecular target data. J. Comput. Chem. 21, 86-104.
21. Fuxreiter, M., Luo, N., Jedlovszky, P., Simon, I. & Osman, R. 2002 Role of base flipping in specific recognition of damaged DNA by repair enzymes. J. Mol. Biol. 323, 823-834.
22. Garcia, R. A., Bustamante, C. J. & Reich, N. O. 1996 Proc. Nati Acad. Sci. USA 93, 7618-7622.
23. Giudice, E., Varnai, P. & Lavery, R. 2001 Energetic and conformational aspects of A:T base pair opening within the DNA double helix. Phys. Chem. Chem. Phys. 2, 673-677.
24. Giudice, E., Varnai, P. & Lavery, R. 2003 Base pair opening within B-DNA: free energy pathways for GC and AT pairs from umbrella sampling simulations. Nucleic Acids Res. 31, 1434-1443.
25. Goedecke, K., Pignot, M., Goody, R. S., Scheidig, A. J. & Weinhold, E. 2001 Structure of the N6-adenine DNA methyltransferase M.TagI in complex with DNA and a cofactor analog. Nat. Struct. Biol. 8, 101-103.
26. Guckian, K. M., Schweitzer, B. A., Ren, R. X.-F., Sheils, C. J., Tahmassebi, D. C. & Kool, E. T. 2000 Factors contributiong to aromatic stacking in water: evaluation in the context of DNA. J. Am. Chem. Soc. 122, 2213-2222.
27. Guéron, M. & Leroy, J. L. 1995 Studies of base pair kinetics by NMR measurement of proton exchange. Meth. Enzymol. 261, 383-413.
28. Guéron, M., Kochoyan, M. & Leroy, J. L. 1987 A single mode of DNA base-pair opening drives imino proton exchange. Nature 328, 89-92.
29. Huang, N., Banavali, N. K. & MacKerell Jr, A. D. 2003 Protein-facilitated base flipping in DNA by cytosine-5-methyltransferase. Proc. Natl Acad. Sci. USA 100, 68-73.
30. Humphrey, W., Dalke, A. & Schulten, K. 1996 VMD: visual molecular dynamics. J. Mol. Graphics 14, 33-38.
31. Jorgensen, W. L. 1983 Theoretical studies of medium effects on conformational equilibria. J. Phys. Chem. 87, 5304-5312.
32. Karplus, M. & Petsko, G. A. 1990 Molecular dynamics simulations in biology. Nature 347, 631-639.
33. Keepers, J. W., Kollman, P. A., Weiner, P. K. & James, T. L. 1982 Molecular mechanical studies of DNA flexibility: coupled backbone torsion angles and base-pair openings. Proc. Natl Acad. Sci. USA 79, 5537-5541.
34. Keepers, J. W., Kollman, P. A. & James. T. L. 1984 Molecular mechanical studies of base-pair opening in d(CGCGC):d(GCGCGC), dG5.dC5, d(TATAT):d(ATATA), and dA5.dT5 in the B and Z forms of DNA. Biopolymers 23, 2499-2511.
35. Klimasauskas, S. & Roberts, R. J. 1995 M.HhaI binds tightly to substrates containing mismatches at the target base. Nucleic Acids Res. 23, 1388-1395.
36. Klimasauskas, S., Kumar, S., Roberts, R. J. & Cheng, X. 1994 HhaI methyltransferase flips its target base out of the DNA helix. Cell 76, 357-369.
37. Klimasauskas, S., Szyperski, T., Serva, S. & Wuthrich, K. 1998 Dynamic modes of the flipped-out cytosine during HhaI methyltransferase-DNA interactions in solution. EMBO J. 17, 317-324.
38. Kumar, S., Bouzida, D., Swendsen, R. H., Kollman, P. A. & Rosenberg, J. M. 1992 The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem. 13, 1011-1021.
39. Lange, C., Wild, C. & Trautner, T. A. 1996 Identification of a subdomain within DNA-(cytosine-G5)-methyltransferases responsible for the recognition of the 5′ part of their DNA target. EMBO J. 15, 1443-1450.
40. Lavery, R. & Sklenar, H. 1997 CURVES5.2: helical analysis of irregular nucleic acids. Laboratoire de biochimie theorique, CNRS URA 77, Institut de Biologie Physico-Chimique, Paris, France. (www.ibpc.fr/UPR9080/ Curindex.html)
41. Leijon, M., Sehlstedt, U., Nielsen, P. E. & Graslund, A. 1997 Unique base-pair breathing dynamics in PNA-DNA hybrids. J. Mol. Biol. 271, 438-455.
42. Leroy, J. L., Kochoyan, M., Huynh-Dinh, T. & Guéron, M. 1988 Characterization of base-pair opening in deoxynucleotide duplexes using catalysed exchange of the imino proton. J. Mol. Biol. 200, 223-238.
43. Lindstrom, J. W. M., Flynn, J. & Reich, N. O. 2000 Reconciling structure and function in HhaI DNA cytosine-C-5 methyltransferase. J. Biol. Chem. 275, 4912-4919.
44. Lyakhov, I. G., Hengen, P. N., Rubens, D. & Schneider, T. D. 2001 The PI phage replication protein RepA contacts an otherwise inaccessible thymine N3 proton by DNA distortion or base flipping. Nucleic Acids Res. 29, 4892-1900.
45. McCammon, J. A. & Karplus, M. 1979 Dynamics of activated processes in globular proteins. Proc. Natl Acad. Sci. USA 76, 3585-3589.
46. MacKerell Jr, A. D. & Banavali, N. 2000 All-atom empirical force field for nucleic acids. 2. Application to molecular dynamics simulations of DNA and RNA in solution. J. Comput Chem. 21, 105-120.
47. MacKerell Jr, A. D., Brooks, B., Brooks III, C. L., Nilsson, L., Roux, B., Won, Y. & Karplus, M. 1998a CHARMM: the energy function and its paramerization with an overview of the program. In Encyclopedia of computational chemistry (ed. P. V. R. Schleyer and others), vol. 1, pp. 271-277. Wiley.
48. MacKerell Jr, A. D. (and 28 others) 19986 All-atom empirical potential for molecular modeling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586-3616.
49. McQuarrie, D. A. 1976 Statistical mechanics. New York: Harper and Row.
50. Mi, S., Alsono, D. & Roberts, R. J. 1995 Functional analysis of Gln237 mutants of HhaI methyltransferase. Nucleic Acids Res. 23, 620-627.
51. Moe, J. G. & Russu, I. M. 1992 Kinetics and energetics of base-pair opening in 5′d(CGCGAA-TTCGCG)-3′ and a substituted dodecamer containing G-T mismatches. Biochemistry 31, 8421-8428.
52. O'Gara, M., Klimasauskas, S., Roberts, R. J. & Cheng, X. 1996a Enzymatic C5-cytosine methylation of DNA: mechanistic implications of new crystal structures for Hha1 methyltransferase-DNA-AdoHcy complexes. J. Mol. Biol. 261, 634-645.
53. O'Gara, M., Roberts, R. J. & Cheng, X. 19966 A structural basis for the preferential binding of hemimethylated DNA by Hha1 DNA methyltransferase. J. Mol. Biol. 263, 597-606.
54. O'Gara, M., Horton, J. R., Roberts, R. J. & Cheng, X. 1998 Structures of Hha1 methyltransferase complexed with substrates containing mismatches at the target base. Nat. Struct. Biol. 5, 872-877.
55. Ramstein, J. & Lavery, R. 1988 Energetic coupling between DNA bending and base pair opening. Proc. Natt Acad. Sci. USA 86, 7231-7235.
56. Rasko, T., Finta, C. & Kiss, A. 2000 DNA bending induced by DNA (cytosine-5) methyltransferases. Nucleic Acids Res. 28, 3083-3091.
57. 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.
58. Roberts, R. J. 1995 On base flipping. Cell 82, 9-12.
59. Roberts, R. J. & Cheng, X. 1998 Base flipping. A. Rev. Biochem. 67, 181-198.
60. Schlick, T. & Strahs, D. 2000 A-Tract bending: insight into experimental structures by computational models. J. Mol. Biol. 301, 643-663.
61. 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, 4881-1891.
62. Slupphaug, G., Mol, C. D., Kavli, B., Arvai, A. S., Krokan, H. E. & Tainer, J. A. 1996 A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature 384, 87-32.
63. Spies, M. A. & Schowen, R. L. 2002 The trapping of a spontaneously 'flipped-out' base from double helical nucleic acids by host-guest complexation with β-cyclodextrin: the intrinsic base-flipping rate constant for DNA and RNA. J. Am. Chem. Soc. 124, 14049-14053.
64. Steinbach, P. J. & Brooks, B. R. 1994 New spherical-cut-off methods of long-range forces in macromolecular simulations. J. Comput. Chem. 15, 667-683.
65. van Aalten, D. M. F., Erlanson, D. A., Verdine, G. L. & Joshua-Tor, L. 1999 A structural snapshot of base-pair opening in DNA. Proc. Natl Acad. Sci. USA 96, 11809-11814.
66. Varnai, P. & Lavery, R. 2002 Base flipping in DNA: pathways and energetics studied with molecular dynamic simulations. J. Am. Chem. Soc. 124, 7272-7273.
67. Vertino, P. M. 1999 Structures and functions. In S-Adenosylmethionine- dependent methyltransferases (ed. X. Cheng & R. M. Blumenthal), pp. 341-372. World Scientific.
68. Vilkaitis, G., Merkiene, E., Serva, S., Weinhold, E. & Klimasauskas, S. 2001 The mechanism of DNA cytosine-5 methylation. J. Biol. Chem. 276, 20924-20934.
69. Winkler, F. K. 1994 DNA totally flipped out by methylase. Structure 2, 79-83.
70. Wu, J. C. & Santi, D. V. 1987 Kinetic and catalytic mechanism of HhaI methyltransferase. J. Biol. Chem. 262, 4778-4786.