Cation binding to 15-TBA quadruplex DNA is a multiple-pathway cation-dependent process

Nucleic Acids Research

Volumn 39, Issue 22, 2011, Pages 9789-9802

  Reshetnikov, Roman V ^a,b   Sponer, Jiri ^c   Rassokhina, Olga I ^a   Kopylov, Alexei M ^a   Tsvetkov, Philipp O ^d   Makarov, Alexander A ^d   Golovin, Andrey V ^a,b  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b Apto Pharm LLC   (Russian Federation)

^c INSTITUTE OF BIOPHYSICS   (Czech Republic)

^d ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; CATION; DNA; GUANINE QUADRUPLEX; POTASSIUM ION; SODIUM ION; THROMBIN BINDING APTAMER; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA BINDING; DNA CONFORMATION; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; QUANTUM YIELD; SIMULATION; STATIC ELECTRICITY;

APTAMERS, NUCLEOTIDE; CALORIMETRY; CATIONS; DNA; G-QUADRUPLEXES; MOLECULAR DYNAMICS SIMULATION; POTASSIUM; SODIUM;

EID: 83755185482     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr639     Document Type: Article

References (81)

1. Gellert,M., Lipsett,M.N. and Davies,D.R. (1962) Helix formation by guanylic acid. Proc. Natl Acad. Sci. USA, 48, 2013-2018.
2. Blackburn,E.H. (1994) Telomeres: no end in sight. Cell, 77, 621-623. (Pubitemid 24175598)
3. De Lange,T. (2005) Telomere-related genome instability in cancer. Cold Spring Harb. Symp. Quant. Biol., 70, 197-204. (Pubitemid 44124872)
4. De Cian,A., Lacroix,L., Douarre,C., Temime-Smaali,N., Trentesaux,C., Riou,J.-F. and Mergny,J.-L. (2008) Targeting telomeres and telomerase. Biochimie, 90, 131-155. (Pubitemid 350245369)
5. Sen,D. and Gilbert,W. (1988) Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature, 334, 364-366.
6. Simonsson,T. (2001) G-quadruplex DNA structures-variations on a theme. Biol. Chem., 382, 621-628.
7. Cogoi,S. and Xodo,L.E. (2006) G-quadruplex formation within the promoter of the KRAS proto-oncogene and its effect on transcription. Nucleic Acids Res., 34, 2536-2549. (Pubitemid 43985618)
8. Rankin,S., Reszka,A.P., Huppert,J., Zloh,M., Parkinson,G.N., Todd,A.K., Ladame,S., Balasubramanian,S. and Neidle,S. (2005) Putative DNA quadruplex formation within the human c-kit oncogene. J. Am. Chem. Soc., 127, 10584-10589. (Pubitemid 41061432)
9. Dexheimer,T.S., Sun,D. and Hurley,L.H. (2006) Deconvoluting the structural and drug-recognition complexity of the G-quadruplex-forming region upstream of the bcl-2 P1 promoter. J. Am. Chem. Soc., 128, 5404-5415.
10. Siddiqui-Jain,A., Grand,C.L., Bearss,D.J. and Hurley,L.H. (2002) Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc. Natl Acad. Sci. USA, 99, 11593-11598. (Pubitemid 34994444)
11. Métifiot,M., Leon,O., Tarrago-Litvak,L., Litvak,S. and Andréola,M.-L. (2005) Targeting HIV-1 integrase with aptamers selected against the purified RNase H domain of HIV-1 RT. Biochimie, 87, 911-919. (Pubitemid 41297818)
12. Bates,P.J., Kahlon,J.B., Thomas,S.D., Trent,J.O. and Miller,D.M. (1999) Antiproliferative Activity of G-rich Oligonucleotides Correlates with Protein Binding. J. Biol. Chem., 274, 26369-26377.
13. Bock,L.C., Griffin,L.C., Latham,J.A., Vermaas,E.H. and Toole,J.J. (1992) Selection of single-stranded DNA molecules that bind and inhibit humanthrombin. Nature, 355, 564-566.
14. Lane,A.N., Chaires,J.B., Gray,R.D. and Trent,J.O. (2008) Stability and kinetics of G-quadruplex structures. Nucleic Acids Res., 36, 5482-5515.
15. Burge,S., Parkinson,G.N., Hazel,P., Todd,A.K. and Neidle,S. (2006) Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res., 34, 5402-5415. (Pubitemid 44742430)
16. Smirnov,I. and Shafer,R.H. (2000) Effect of loop sequence and size on DNA aptamer stability. Biochemistry, 39, 1462-1468. (Pubitemid 30090716)
17. Hazel,P., Huppert,J., Balasubramanian,S. and Neidle,S. (2004) Loop-length-dependent folding of G-quadruplexes. J. Am. Chem. Soc., 126, 16405-16415. (Pubitemid 40081938)
18. Smargiasso,N., Rosu,F., Hsia,W., Colson,P., Baker,E.S., Bowers,M.T., De Pauw,E. and Gabelica,V. (2008) G-quadruplex DNA assemblies: loop length, cation identity, and multimer formation. J. Am. Chem. Soc., 130, 10208-10216.
19. Guédin,A., Gros,J., Alberti,P. and Mergny,J.-L. (2010) How long is too long? Effects of loop size on G-quadruplex stability. Nucleic Acids Res., 38, 7858-7868.
20. Risitano,A. and Fox,K.R. (2004) Influence of loop size on the stability of intramolecular DNA quadruplexes. Nucleic Acids Res., 32, 2598-2606. (Pubitemid 38854813)
21. Pinnavaia,T.J., Marshall,C.L., Mettler,C.M., Fisk,C.L., Miles,H.T. and Becker,E.D. (1978) Alkali metal ion specificity in the solution ordering of a nucleotide, 5'-guanosine monophosphate. J. Am. Chem. Soc., 100, 3625-3627.
22. Chen,F.M. (1992) Strontium(2+) facilitates intermolecular G-quadruplex formation of telomeric sequences. Biochemistry, 31, 3769-3776.
23. Smirnov,I. and Shafer,R.H. (2000) Lead is unusually effective in sequence-specific folding of DNA. J. Mol. Biol., 296, 1-5.
24. Phillips,K., Dauter,Z., Murchie,A.I., Lilley,D.M. and Luisi,B. (1997) The crystal structure of a parallel-stranded guanine tetraplex at 0.95 A resolution. J. Mol. Biol., 273, 171-182. (Pubitemid 27460223)
25. Ida,R. and Wu,G. (2008) Direct NMR detection of alkali metal ions bound to G-quadruplex DNA. J. Am. Chem. Soc., 130, 3590-3602. (Pubitemid 351456063)
26. Sket,P. and Plavec,J. (2010) Tetramolecular DNA quadruplexes in solution: insights into structural diversity and cation movement. J. Am. Chem. Soc., 132, 12724-12732.
27. Hud,N.V., Schultze,P., Sklenář,V. and Feigon,J. (1999) Binding sites and dynamics of ammonium ions in a telomere repeat DNA quadruplex. J. Mol. Biol., 285, 233-243. (Pubitemid 29034040)
28. Štefl,R., Cheatham,T.E., Špačková,N., Fadrná,E., Berger,I., Koča,J. and Šponer,J. (2003) Formation pathways of a guanine-quadruplex DNA revealed by molecular dynamics and thermodynamic analysis of the substates. Biophys. J., 85, 1787-1804. (Pubitemid 37052261)
29. Špačková,N., Berger,I. and Šponer,J. (1999) Nanosecond molecular dynamics simulations of parallel and antiparallel guanine quadruplex DNA molecules. J. Am. Chem. Soc., 121, 5519-5534.
30. Špačková,N., Berger,I. and Šponer,J. (2001) Structural dynamics and cation interactions of DNA quadruplex molecules containing mixed guanine/cytosine quartets revealed by large-scale MD simulations. J. Am. Chem. Soc., 123, 3295-3307. (Pubitemid 32884618)
31. Šponer,J. and Špačková,N. (2007) Molecular dynamics simulations and their application to four-stranded DNA. Methods, 43, 278-290. (Pubitemid 47633206)
32. Li,M.-H., Zhou,Y.-H., Luo,Q. and Li,Z.-S. (2010) The 3D structures of G-quadruplexes of HIV-1 integrase inhibitors: molecular dynamics simulations in aqueous solution and in the gas phase. J. Mol. Model, 16, 645-657.
33. Cavallari,M., Calzolari,A., Garbesi,A. and Di Felice,R. (2006) Stability and migration of metal ions in G4-wires by molecular dynamics simulations. J. Phys. Chem. B, 110, 26337-26348. (Pubitemid 46133356)
34. Cavallari,M., Garbesi,A. and Di Felice,R. (2009) Porphyrin intercalation in G4-DNA quadruplexes by molecular dynamics simulations. J. Phys. Chem. B, 113, 13152-13160.
35. Hazel,P., Parkinson,G.N. and Neidle,S. (2006) Predictive modelling of topology and loop variations in dimeric DNA quadruplex structures. Nucleic Acids Res., 34, 2117-2127. (Pubitemid 44314209)
36. Rueda,M., Luque,F.J. and Orozco,M. (2006) G-quadruplexes can maintain their structure in the gas phase. J. Am. Chem. Soc., 128, 3608-3619.
37. Li,H., Cao,E.-hua and Gisler,T. (2009) Force-induced unfolding of human telomeric G-quadruplex: a steered molecular dynamics simulation study. Biochem. Biophys. Res. Commun., 379, 70-75.
38. Pagano,B., Mattia,C.A., Cavallo,L., Uesugi,S., Giancola,C. and Fraternali,F. (2008) Stability and cations coordination of DNA and RNA 14-mer G-quadruplexes: a multiscale computational approach. J. Phys. Chem. B, 112, 12115-12123.
39. Haider,S. and Neidle,S. (2010) Molecular modeling and simulation of G-quadruplexes and quadruplex-ligand complexes. Methods Mol. Biol., 608, 17-37.
40. Petraccone,L., Garbett,N.C., Chaires,J.B. and Trent,J.O. (2010) An integrated molecular dynamics (MD) and experimental study of higher order human telomeric quadruplexes. Biopolymers, 93, 533-548.
41. Reshetnikov,R., Golovin,A., Spiridonova,V., Kopylov,A. and Šponer,J. (2010) Structural dynamics of thrombin-binding DNA aptamer d(GGTTGGTGTGGTTGG) quadruplex DNA studied by large-scale explicit solvent simulations. J. Chem. Theory Comput., 6, 3003-3014.
42. Pérez,A., Marchán,I., Svozil,D., Sponer,J., Cheatham,T.E., Laughton,C.A. and Orozco,M. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of a/g conformers. Biophys. J., 92, 3817-3829. (Pubitemid 46910569)
43. Fadrná,E., Špačková,N., Sarzyñska,J., Koča,J., Orozco,M., Cheatham,T.E., Kulinski,T. and Šponer,J. (2009) Single stranded loops of quadruplex DNA as key benchmark for testing nucleic acids force fields. J. Chem. Theory Comput., 5, 2514-2530.
44. Schultze,P., Macaya,R.F. and Feigon,J. (1994) Three-dimensional Solution Structure of the Thrombin-binding DNA Aptamer d(GG TTGGTGTGGTTGG). J. Mol. Biol., 235, 1532-1547. (Pubitemid 24150403)
45. Mao,X., Marky,L.A. and Gmeiner,W.H. (2004) NMR structure of the thrombin-binding DNA aptamer stabilized by Sr2+. J. Biomol. Struct. Dyn., 22, 25-33. (Pubitemid 39095279)
46. Marathias,V.M. and Bolton,P.H. (1999) Determinants of DNA quadruplex structural type: sequence and potassium binding. Biochemistry, 38, 4355-4364.
47. Marathias,V.M. and Bolton,P.H. (2000) Structures of the potassium-saturated, 2:1, and intermediate, 1:1, forms of a quadruplex DNA. Nucleic Acids Res., 28, 1969-1977. (Pubitemid 30229664)
48. Trajkovski,M., Šket,P. and Plavec,J. (2009) Cation localization and movement within DNA thrombin binding aptamer in solution. Org. Biomol. Chem., 7, 4677.
49. Jing,N., Marchand,C., Liu,J., Mitra,R., Hogan,M.E. and Pommier,Y. (2000) Mechanism of inhibition of HIV-1 integrase by G-tetrad-forming oligonucleotides in Vitro. J. Biol. Chem., 275, 21460-21467. (Pubitemid 30481849)
50. Cordomì,A., Edholm,O. and Perez,J.J. (2009) Effect of Force Field Parameters on Sodium and Potassium Ion Binding to Dipalmitoyl Phosphatidylcholine Bilayers. J. Chem. Theory Comput., 5, 2125-2134.
51. van der Spoel,D., Lindahl,E., Hess,B., Groenhof,G., Mark,A.E. and Berendsen,H.J.C. (2005) GROMACS: fast, flexible, and free. J. Comput. Chem., 26, 1701-1718. (Pubitemid 43076182)
52. Hess,B., Kutzner,C., van der Spoel,D. and Lindahl,E. (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Comput. Chem., 4, 435-447.
53. Bussi,G., Donadio,D. and Parrinello,M. (2007) Canonical sampling through velocity rescaling. J. Chem. Phys., 126, 014101-014107.
54. Berendsen,H.J.C., Postma,J.P.M., van Gunsteren,W.F., DiNola,A. and Haak,J.R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys., 81, 3684-3690.
55. Darden,T., York,D. and Pedersen,L. (1993) Particle mesh Ewald: An Nlog(N) method for Ewald sums in large systems. J. Chem. Phys., 98, 10089-10092.
56. Jorgensen,W.L., Chandrasekhar,J., Madura,J.D., Impey,R.W. and Klein,M.L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys., 79, 926-935.
57. Joung,I.S. and Cheatham. (2008) Determination of alkali and halide monovalent ion parameters for use in explicitly solvated biomolecular simulations. J. Phys. Chem. B, 112, 9020-9041.
58. Kankia,B.I. and Marky,L.A. (2001) Folding of the thrombin aptamer into a G-quadruplex with Sr(2+): stability, heat, and hydration. J. Am. Chem. Soc., 123, 10799-10804. (Pubitemid 33041990)
59. Payne,M., Teter,M., Allan,D., Arias,T. and Joannopoulos,J. (1992) Iterative minimization techniques for ab initio total-energy calculations: molecular dynamics and conjugate gradients. Rev. Mod. Phys., 64, 1045.
60. Pant,M.M. and Rajagopal,A.K. (1972) Theory of inhomogeneous magnetic electron gas. Solid State Commun., 10, 1157-1160.
61. Perdew,J.P., Chevary,J.A., Vosko,S.H., Jackson,K.A., Pederson,M.R., Singh,D.J. and Fiolhais,C. (1992) Atoms, molecules, solids, and surfaces: Applications of the generalized gradient approximation for exchange and correlation. Phys. Rev. B, 46, 6671.
62. Vanderbilt,D. (1990) Soft self-consistent pseudopotentials in a generalized eigenvalue formalism. Phys. Rev. B, 41, 7892.
63. Grimme,S. (2004) Accurate description of van der Waals complexes by density functional theory including empirical corrections. J. Comput. Chem., 25, 1463-1473.
64. Biswas,P.K. and Gogonea,V. (2005) A regularized and renormalized electrostatic coupling Hamiltonian for hybrid quantum-mechanical-molecular- mechanical calculations. J. Chem. Phys., 123, 164114.
65. Nosé,S. (1984) A molecular dynamics method for simulations in the canonical ensemble. Mol. Phys., 52, 255.
66. Hoover,W.G. (1985) Canonical dynamics: equilibrium phase-space distributions. Phys. Rev. A, 31, 1695.
67. Tsvetkov,P.O., Devred,F. and Makarov,A.A. (2010) Thermodynamics of zinc binding to human S100A2. Mol. Biol., 44, 832-835.
68. Faralli,C., Pagliai,M., Cardini,G. and Schettino,V. (2007) The solvation dynamics of Na+ and K+ ions in liquid methanol. Theor. Chem. Account, 118, 417-423.
69. Hancock,R.D., Siddons,C.J., Oscarson,K.A. and Reibenspies,J.M. (2004) The structure of the 11-coordinate barium complex of the pendant-donor macrocycle 1,4,7,10-tetrakis(carbamoylmethyl)- 1,4,7,10-tetraazacyclododecane: an analysis of the coordination numbers of barium(II) in its complexes. Inorg. Chim. Acta, 357, 723-727.
70. Hong,E.S., Yoon,H.-J., Kim,B., Yim,Y.-H., So,H.-Y. and Shin,S.K. (2010) Mass spectrometric studies of alkali metal ion binding on thrombin-binding aptamer DNA. J. Am. Soc. Mass Spectrom., 21, 1245-1255.
71. Shim,J.W., Tan,Q. and Gu,L.-Q. (2009) Single-molecule detection of folding and unfolding of the G-quadruplex aptamer in a nanopore nanocavity. Nucleic Acids Res., 37, 972-982.
72. Vairamani,M. and Gross,M.L. (2003) G-quadruplex formation of thrombin-binding aptamer detected by electrospray ionization mass spectrometry. J. Am. Chem. Soc., 125, 42-43. (Pubitemid 36068639)
73. Fadrná,E., Špačková,N., Štefl,R., Koča,J., Cheatham,T.E. and Šponer,J. (2004) Molecular dynamics simulations of guanine quadruplex loops: advances and force field limitations. Biophys. J., 87, 227-242. (Pubitemid 38880080)
74. Zacharias,M. (2000) Simulation of the structure and dynamics of nonhelical RNA motifs. Curr. Opin. Struct. Biol., 10, 311-317. (Pubitemid 30333100)
75. Perahia,D., Pullman,A. and Pullman,B. (1976) Cation-binding to biomolecules. Theoret. Chim. Acta, 42, 23-31.
76. Turjanski,A.G., Hummer,G. and Gutkind,J.S. (2009) How mitogen-activated protein kinases recognize and phosphorylate their targets: a QM/MM study. J. Am. Chem. Soc., 131, 6141-6148.
77. Banás,P., Jurecka,P., Walter,N.G., Sponer,J. and Otyepka,M. (2009) Theoretical studies of RNA catalysis: Hybrid QM/MM methods and their comparison with MD and QM. Methods, 49, 202-216.
78. Nagatoishi,S., Tanaka,Y. and Tsumoto,K. (2007) Circular dichroism spectra demonstrate formation of the thrombin-binding DNA aptamer G-quadruplex under stabilizing-cation-deficient conditions. Biochem. Biophys. Res. Commun., 352, 812-817. (Pubitemid 44880327)
79. Fadrná,E., Špačková,N., Štefl,R., Koča,J., Cheatham,T.E. and Šponer,J. (2004) Molecular dynamics simulations of guanine quadruplex loops: advances and force field limitations. Biophys. J., 87, 227-242. (Pubitemid 38880080)
80. Cang,X., Šponer,J. and Cheatham,T.E. (2011) Explaining the varied glycosidic conformational, G-tract length and sequence preferences for anti-parallel G-quadruplexes. Nucleic Acids Res., 39, 4499-4512.
81. Zacharias,M. (2000) Simulation of the structure and dynamics of nonhelical RNA motifs. Curr. Opin. Struct. Biol., 10, 311-317. (Pubitemid 30333100)