Mg2+ in the major groove modulates b-dna structure and dynamics

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Guéroult, Marc ^a,b   Boittin, Olivier ^a   Mauffret, Oliver ^c   Etchebest, Catherine ^a   Hartmann, Brigitte ^a,c  

^a hôpital Robert Debré et Institut national de la transfusion sanguine   (France)

^b INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^c Ecole Normale Superieure de Cachan   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA B; MAGNESIUM ION; OLIGOMER; PHOSPHATE; MAGNESIUM;

5' UNTRANSLATED REGION; ARTICLE; CONFORMATION; CRYSTALLOGRAPHY; DNA DETERMINATION; DNA STRUCTURE; HYDROGEN BOND; MODULATION; MOLECULAR DYNAMICS; PROTEIN DNA BINDING; STATIC ELECTRICITY; CHEMISTRY; DRUG EFFECT; METABOLISM; MOLECULAR DOCKING; NUCLEOSOME; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; DNA, B-FORM; MAGNESIUM; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; NUCLEIC ACID CONFORMATION; NUCLEOSOMES; STATIC ELECTRICITY;

EID: 84864260157     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041704     Document Type: Article

References (62)

1. Egli M, (2002) DNA-cation interactions: quo vadis? Chem Biol 9: 277-286.
2. Hud NV, Polak M, (2001) DNA-cation interactions: The major and minor grooves are flexible ionophores. Curr Opin Struct Biol 11: 293-301.
3. Subirana JA, Soler-Lopez M, (2003) Cations as hydrogen bond donors: a view of electrostatic interactions in DNA. Annu Rev Biophys Biomol Struct 32: 27-45.
4. Ponomarev SY, Thayer KM, Beveridge DL, (2004) Ion motions in molecular dynamics simulations on DNA. Proc Natl Acad Sci U S A 101: 14771-14775.
5. Bai Y, Greenfeld M, Travers KJ, Chu VB, Lipfert J, et al. (2007) Quantitative and comprehensive decomposition of the ion atmosphere around nucleic acids. J Am Chem Soc 129: 14981-14988.
6. Abrescia NG, Malinina L, Fernandez LG, Huynh-Dinh T, Neidle S, et al. (1999) Structure of the oligonucleotide d(CGTATATACG) as a site-specific complex with nickel ions. Nucleic Acids Res 27: 1593-1599.
7. Chiu TK, Dickerson RE, (2000) 1 A crystal structures of B-DNA reveal sequence-specific binding and groove-specific bending of DNA by magnesium and calcium. J Mol Biol 301: 915-945.
8. Grzeskowiak K, Goodsell DS, Kaczor-Grzeskowiak M, Cascio D, Dickerson RE, (1993) Crystallographic analysis of C-C-A-A-G-C-T-T-G-G and its implications for bending in B-DNA. Biochemistry 32: 8923-8931.
9. Kielkopf CL, Ding S, Kuhn P, Rees DC, (2000) Conformational flexibility of B-DNA at 0.74 A resolution: d(CCAGTACTGG)(2). J Mol Biol 296: 787-801.
10. Liu J, Subirana JA, (1999) Structure of d(CGCGAATTCGCG) in the presence of Ca(2+) ions. J Biol Chem 274: 24749-24752.
11. Mack DR, Chiu TK, Dickerson RE, (2001) Intrinsic bending and deformability at the T-A step of CCTTTAAAGG: a comparative analysis of T-A and A-T steps within A-tracts. J Mol Biol 312: 1037-1049.
12. Millonig H, Pous J, Gouyette C, Subirana JA, Campos JL, (2009) The interaction of manganese ions with DNA. J Inorg Biochem 103: 876-880.
13. Minasov G, Tereshko V, Egli M, (1999) Atomic-resolution crystal structures of B-DNA reveal specific influences of divalent metal ions on conformation and packing. J Mol Biol 291: 83-99.
14. Soler-Lopez M, Malinina L, Subirana JA, (2000) Solvent organization in an oligonucleotide crystal. The structure of d(GCGAATTCG)2 at atomic resolution. J Biol Chem 275: 23034-23044.
15. Varnai P, Timsit Y, (2010) Differential stability of DNA crossovers in solution mediated by divalent cations. Nucleic Acids Res 38: 4163-4172.
16. Hud NV, Schultze P, Sklenar V, Feigon J, (1999) Binding sites and dynamics of ammonium ions in a telomere repeat DNA quadruplex. J Mol Biol 285: 233-243.
17. Hud NV, Sklenar V, Feigon J, (1999) Localization of ammonium ions in the minor groove of DNA duplexes in solution and the origin of DNA A-tract bending. J Mol Biol 286: 651-660.
18. Quintana JR, Grzeskowiak K, Yanagi K, Dickerson RE, (1992) Structure of a B-DNA decamer with a central T-A step: C-G-A-T-T-A-A-T-C-G. J Mol Biol 225: 379-395.
19. Pullman A, Pullman B, (1981) Molecular electrostatic potential of the nucleic acids. Quarterly reviews of biophysics 14: 289-380.
20. Srinivasan AR, Sauers RR, Fenley MO, Boschitsch AH, Matsumoto A, et al. (2009) Properties of the Nucleic-acid Bases in Free and Watson-Crick Hydrogen-bonded States: Computational Insights into the Sequence-dependent Features of Double-helical DNA. Biophys Rev 1: 13-20.
21. Moldrheim E, Andersen B, Froystein NA, Sletten E, (1998) Interaction of manganese(II), cobalt(II) and nickel(II) with DNA oligomers studied by 1H NMR spectroscopy. Inorganica Chimica Acta 273: 41-46.
22. Froystein N, Davis J, Reid B, Sletten E, (1993) Sequence-selective metal ion binding to DNA oligonucleotides. Acta Chem Scand 47: 49-57.
23. Froystein N, Sletten E, (1991) The Binding of Manganese and Zinc to the Synthetic Oligonucleotide d(CGCGAATTCGCG). A 1H NMR Study. Acta chemica scandinavica 45: 219-225.
24. Steinkopf S, Sletten E, (1994) Sequence-selective metal ion binding to DNA hexamers. Acta Chem Scand 48: 388-392.
25. Tereshko V, Minasov G, Egli M, (1998) The Dickerson-Drew B-DNA Dodecamer Revisited at Atomic Resolution. Journal of the American Chemical Society 121: 470-471.
26. Ahmad R, Arakawa H, Tajmir-Riahi HA, (2003) A comparative study of DNA complexation with Mg(II) and Ca(II) in aqueous solution: major and minor grooves bindings. Biophys J 84: 2460-2466.
27. Chiu TK, Kaczor-Grzeskowiak M, Dickerson RE, (1999) Absence of minor groove monovalent cations in the crosslinked dodecamer C-G-C-G-A-A-T-T-C-G-C-G. J Mol Biol 292: 589-608.
28. Brukner I, Susic S, Dlakic M, Savic A, Pongor S, (1994) Physiological concentration of magnesium ions induces a strong macroscopic curvature in GGGCCC-containing DNA. J Mol Biol 236: 26-32.
29. Han W, Dlakic M, Zhu YJ, Lindsay SM, Harrington RE, (1997) Strained DNA is kinked by low concentrations of Zn2+. Proc Natl Acad Sci U S A 94: 10565-10570.
30. Jerkovic B, Bolton PH, (2001) Magnesium increases the curvature of duplex DNA that contains dA tracts. Biochemistry 40: 9406-9411.
31. Abi-Ghanem J, Heddi B, Foloppe N, Hartmann B, (2010) DNA structures from phosphate chemical shifts. Nucleic Acids Res 38: e18.
32. Heddi B, Foloppe N, Bouchemal N, Hantz E, Hartmann B, (2006) Quantification of DNA BI/BII backbone states in solution. Implications for DNA overall structure and recognition. J Am Chem Soc 128: 9170-9177.
33. Heddi B, Foloppe N, Hantz E, Hartmann B, (2007) The DNA structure responds differently to physiological concentrations of K(+) or Na(+). J Mol Biol 368: 1403-1411.
34. Heddi B, Foloppe N, Oguey C, Hartmann B, (2008) Importance of accurate DNA structures in solution: the Jun-Fos model. J Mol Biol 382: 956-970.
35. Djuranovic D, Hartmann B, (2003) Conformational characteristics and correlations in crystal structures of nucleic acid oligonucleotides: evidence for sub-states. J Biomol Struct Dyn 20: 771-788.
36. Djuranovic D, Hartmann B, (2004) DNA fine structure and dynamics in crystals and in solution: the impact of BI/BII backbone conformations. Biopolymers 73: 356-368.
37. Grzeskowiak K, Yanagi K, Prive GG, Dickerson RE, (1991) The structure of B-helical C-G-A-T-C-G-A-T-C-G and comparison with C-C-A-A-C-G-T-T-G-G. The effect of base pair reversals. Journal of Biological Chemistry 266: 8861-8883.
38. Hartmann B, Piazzola D, Lavery R, (1993) BI-BII transitions in B-DNA. Nucleic Acids Res 21: 561-568.
39. Oguey C, Foloppe N, Hartmann B, (2010) Understanding the sequence-dependence of DNA groove dimensions: implications for DNA interactions. PLoS One 5: e15931.
40. van Dam L, Levitt MH, (2000) BII nucleotides in the B and C forms of natural-sequence polymeric DNA: A new model for the C form of DNA. J Mol Biol 304: 541-561.
41. Winger RH, Liedl KR, Pichler A, Hallbrucker A, Mayer E, (1999) Helix morphology changes in B-DNA induced by spontaneous B(I)& = = >B(II) substrate interconversion. J Biomol Struct Dyn 17: 223-235.
42. Heddi B, Oguey C, Lavelle C, Foloppe N, Hartmann B, (2010) Intrinsic flexibility of B-DNA: the experimental TRX scale. Nucleic Acids Res 38: 1034-1047.
43. Auffinger P, Grover N, Westhof E, (2011) Metal ion binding to RNA. Met Ions Life Sci 9: 1-35.
44. Draper DE, Grilley D, Soto AM, (2005) Ions and RNA folding. Annual review of biophysics and biomolecular structure 34: 221-243.
45. Joli F, Bouchemal N, Laigle A, Hartmann B, Hantz E, (2006) Solution structure of a purine rich hexaloop hairpin belonging to PGY/MDR1 mRNA and targeted by antisense oligonucleotides. Nucleic Acids Res 34: 5740-5751.
46. Young MA, Beveridge DL, (1998) Molecular dynamics simulations of an oligonucleotide duplex with adenine tracts phased by a full helix turn. J Mol Biol 281: 675-687.
47. Auffinger P, Westhof E, (2000) Water and ion binding around RNA and DNA (C, G) oligomers. J Mol Biol 300: 1113-1131.
48. Varnai P, Zakrzewska K, (2004) DNA and its counterions: a molecular dynamics study. Nucleic Acids Res 32: 4269-4280.
49. Richmond TJ, Davey CA, (2003) The structure of DNA in the nucleosome core. Nature 423: 145-150.
50. Davey CA, Richmond TJ, (2002) DNA-dependent divalent cation binding in the nucleosome core particle. Proc Natl Acad Sci U S A 99: 11169-11174.
51. Wu B, Davey CA, (2010) Using soft X-rays for a detailed picture of divalent metal binding in the nucleosome. J Mol Biol 398: 633-640.
52. Case DA, Cheatham TE 3rd, Darden T, Gohlke H, Luo R, et al (2005) The Amber biomolecular simulation programs. J Comput Chem 26: 1668-1688.
53. Cheatham TE 3rd, Cieplak P, Kollman PA (1999) A modified version of the Cornellet al. force field with improved sugar pucker phases and helical repeat. J Biomol Struct Dyn 16: 845-862.
54. Dixit SB, Beveridge DL, Case DA, Cheatham TE 3rd, Giudice E, et al (2005) Molecular dynamics simulations of the 136 unique tetranucleotide sequences of DNA oligonucleotides. II: sequence context effects on the dynamical structures of the 10 unique dinucleotide steps. Biophys J 89: 3721-3740.
55. Perez A, Marchan I, Svozil D, Sponer J, Cheatham TE 3rd, et al (2007) Refinement of the AMBER force field for nucleic acids: improving the description of [alpha]/[gamma] conformers. Biophysical journal 92: 3817-3829.
56. Lankas F, Spackova N, Moakher M, Enkhbayar P, Sponer J, (2010) A measure of bending in nucleic acids structures applied to A-tract DNA. Nucleic Acids Res 38: 3414-3422.
57. Jorgensen WL, Chandrasekhar J, Madura JD, (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79: 926-935.
58. Berendsen HJC, Postma WF, Van Gunsteren A, DiNola A, Haak JR, (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81: 3684-3690.
59. Ryckaert J, Ciccotti G, Berendsen H, (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J comput Phys 23: 327-341.
60. Cheatham TE III, Miller JL, Fox T, Darden TA, Kollman PA, (1995) Molecular Dynamics Simulations on Solvated Biomolecular Systems: The Particle Mesh Ewald Method Leads to Stable Trajectories of DNA, RNA, and Proteins. Journal of the American Chemical Society 117: 4193-4194.
61. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA, (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041.
62. Lavery R, Moakher M, Maddocks JH, Petkeviciute D, Zakrzewska K, (2009) Conformational analysis of nucleic acids revisited: Curves+. Nucleic Acids Res 37: 5917-5929.