Conformational dynamics of the human propeller telomeric DNA quadruplex on a microsecond time scale

Nucleic Acids Research

Volumn 41, Issue 4, 2013, Pages 2723-2735

  Islam, Barira ^a   Sgobba, Miriam ^a   Laughton, Charlie ^b   Orozco, Modesto ^c   Sponer, Jiri ^d,e   Neidle, Stephen ^f   Haider, Shozeb ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^d INSTITUTE OF BIOPHYSICS   (Czech Republic)

^e CENTRAL EUROPEAN INSTITUTE OF TECHNOLOGY   (Czech Republic)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE QUADRUPLEX;

ARTICLE; CRYSTAL STRUCTURE; DNA CONFORMATION; DNA SEQUENCE; HUMAN; HYDROGEN BOND; LIGAND BINDING; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; STRUCTURE ANALYSIS;

CLUSTER ANALYSIS; DNA; G-QUADRUPLEXES; HUMANS; MOLECULAR DYNAMICS SIMULATION; POTASSIUM; TELOMERE; WATER;

EID: 84876390933     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1331     Document Type: Article

References (72)

1. O'Sullivan, R.J. and Karlseder, J. (2010) Telomeres: protecting chromosomes against genome instability. Nature Rev. Mol. Cell Biol., 11, 171-181.
2. Saldanha, S.N., Andrews, L.G. and Tollefsbol, T.O. (2003) Assessment of telomere length and factors that contribute to its stability. Eur. J. Biochem., 270, 389-403.
3. Sahin, E. and DePinho, R.A. (2012) Axis of ageing: telomeres, p53 and mitochondria. Nature Rev. Mol. Cell Biol., 13, 397-404.
4. Neidle, S. and Parkinson, G.N. (2003) The structure of telomeric DNA. Curr. Opin. Struct. Biol., 13, 275-283.
5. Neidle, S. (2012) Therapeutic Applications of Quadruplex Nucleic Acids. Academic Press, Boston, MA, pp. 109-117.
6. Adrian, M., Heddi, B. and Phan, A.T. (2012) NMR spectroscopy of G-quadruplexes. Methods, 57, 11-24.
7. Gray, R.D. and Chaires, J.B. (2012) Isothermal folding of G-quadruplexes. Methods, 57, 47-55.
8. Randazzo, A., Spada, G. and Silva, M. (2012) Topics in Current Chemistry. Springer, Berlin/Heidelberg, pp. 1-20.
9. Yuan, G., Zhang, Q., Zhou, J. and Li, H. (2011) Mass spectrometry of G-quadruplex DNA: formation, recognition, property, conversion, and conformation. Mass Spectrom. Rev., 30, 1121-1142.
10. Parkinson, G.N., Lee, M.P.H. and Neidle, S. (2002) Crystal structure of parallel quadruplexes from human telomeric DNA. Nature, 417, 876-880.
11. 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.
12. Heddi, B. and Phan, A.T. (2011) Structure of human telomeric DNA in crowded solution. J. Am. Chem. Soc., 133, 9824-9833.
13. Hud, N.V. and Plavec, J. (2006) In: Neidle, S. and Balasubramanian, S. (eds), Quadruplex Nucleic Acids. The Royal Society of Chemistry, pp. 100-130.
14. Ellis, R.J. and Minton, A.P. (2003) Cell biology: join the crowd. Nature, 425, 27-28.
15. Xue, Y., Kan, Z.Y., Wang, Q., Yao, Y., Liu, J., Hao, Y.H. and Tan, Z. (2007) Human telomeric DNA forms parallel-stranded intramolecular G-quadruplex in K+solution under molecular crowding condition. J. Am. Chem. Soc., 129, 11185-11191.
16. Parkinson, G.N., Cuenca, F. and Neidle, S. (2008) Topology conservation and loop flexibility in quadruplex-drug recognition: crystal structures of inter- and intramolecular telomeric DNA quadruplex-drug complexes. J. Mol. Biol., 381, 1145-1156.
17. Neidle, S. (2009) The structures of quadruplex nucleic acids and their drug complexes. Curr. Opin. Struct. Biol., 19, 239-250.
18. Haider, S.M., Autiero, I. and Neidle, S. (2011) Surface area accessibility and the preferred topology of telomeric DNA quadruplex-ligand complexes. Biochimie, 93, 1275-1279.
19. Reshetnikov, R.V., Sponer, J., Rassokhina, O.I., Kopylov, A.M., Tsvetkov, P.O., Makarov, A.A. and Golovin, A.V. (2011) Cation binding to 15-TBA quadruplex DNA is a multiple-pathway cation-dependent process. Nucleic Acids Res., 39, 9789-9802.
20. Haider, S., Parkinson, G.N. and Neidle, S. (2008) Molecular dynamics and principal components analysis of human telomeric quadruplex multimers. Biophys. J., 95, 296-311.
21. Šponer, J., Cang, X. and Cheatham, T.E. III (2012) Molecular dynamics simulations of G-DNA and perspectives on the simulation of nucleic acid structures. Methods, 57, 25-39.
22. Neidle, S. and Parkinson, G.N. (2008) Quadruplex DNA crystal structures and drug design. Biochimie, 90, 1184-1196.
23. Fadrna , E., Spacková , N.a., Sarzyñska, J., Koč a, J., Orozco, M., Cheatham, T.E. III, 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.
24. Perez, A., Luque, F.J. and Orozco, M. (2007) Dynamics of B-DNA on the microsecond time scale. J. Am. Chem. Soc., 129, 14739-14745.
25. 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.
26. Bana s, P., Sklenovský, P., Wedekind, J.E., Šponer, J. and Otyepka, M. (2012) Molecular mechanism of preQ1 riboswitch action: a molecular dynamics study. J. Phys. Chem. B, 116, 12721-12734.
27. Perez, A., Luque, F.J. and Orozco, M. (2011) Frontiers in molecular dynamics simulations of DNA. Acc. Chem. Res., 45, 196-205.
28. Stebbeds, W.J.D., Lunec, J. and Larcombe, L.D. (2012) An in silico study of the differential effect of oxidation on two biologically relevant G-quadruplexes: possible implications in oncogene expression. PLoS One, 7, e43735.
29. Perez, A., Marchan, I., Svozil, D., Sponer, J., Cheatham, T.E. III, Laughton, C.A. and Orozco, M. (2007) Refinement of the AMBER force field for nucleic acids: improving the description of alpha/ gamma conformers. Biophys. J., 92, 3817-3829.
30. Pearlman, D.A., Case, D.A., Caldwell, J.W., Ross, W.S., Cheatham, T.E. III, DeBolt, S., Ferguson, D., Seibel, G. and Kollman, P. (1995) AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput. Phys. Commun., 91, 1-41.
31. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K.M., Ferguson, D.M., Spellmeyer, D.C., Fox, T., Caldwell, J.W. and Kollman, P.A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc., 117, 5179-5197.
32. 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.
33. Darden, T., York, D. and Pedersen, L. (1993) Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems. J. Phys. Chem., 98, 10089-10092.
34. Ryckaert, J.-P., Ciccotti, G. and Berendsen, H.J.C. (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.
35. Case, D.A., Cheatham, T.E. III, Darden, T., Gohlke, H., Luo, R., Merz, K.M., Onufriev, A., Simmerling, C., Wang, B. and Woods, R.J. (2005) The Amber biomolecular simulation programs. J. Comput. Chem., 26, 1668-1688.
36. Bock, H.H. (1996) Probabilistic models in cluster analysis. Comput. Stat. Data Anal., 23, 5-28.
37. Altona, C. and Sundaralingam, M. (1972) Conformational analysis of the sugar ring in nucleosides and nucleotides. A new description using the concept of pseudorotation. J. Am. Chem. Soc., 94, 8205-8212.
38. Humphrey, W., Dalke, A. and Schulten, K. (1996) VMD: visual molecular dynamics. J. Mol. Graph., 14, 33-38.
39. Cang, X., Šponer, J.i. and Cheatham, T.E. III (2011) Insight into G-DNA structural polymorphism and folding from sequence and loop connectivity through free energy analysis. J. Am. Chem. Soc., 133, 14270-14279.
40. Agrawal, S., Ojha, R.P. and Maiti, S. (2008) Energetics of the human Tel-22 quadruplex-telomestatin interaction: a molecular dynamics study. J. Phys. Chem. B, 112, 6828-6836.
41. Akhshi, P., Acton, G. and Wu, G. (2012) Molecular dynamics simulations to provide new insights into the asymmetrical ammonium ion movement inside of the [d(G3T4G4)]2 g-quadruplex DNA structure. J. Phys. Chem. B, 116, 9363-9370.
42. 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.
43. Arora, K. and Schlick, T. (2003) Deoxyadenosine sugar puckering pathway simulated by the stochastic difference equation algorithm. Chem. Phys. Lett., 378, 1-8.
44. Lavery, R., Zakrzewska, K., Beveridge, D., Bishop, T.C., Case, D.A., Cheatham, T.E. III, Dixit, S., Jayaram, B., Lankas, F., Laughton, C. et al. (2010) A systematic molecular dynamics study of nearest-neighbor effects on base pair and base pair step conformations and fluctuations in B-DNA. Nucleic Acids Res., 38, 299-313.
45. Mura, C. and McCammon, J.A. (2008) Molecular dynamics of a kappaB DNA element: base flipping via cross-strand intercalative stacking in a microsecond-scale simulation. Nucleic Acids Res., 36, 4941-4955.
46. Madhumalar, A. and Bansal, M. (2005) Sequence preference for BI/BII conformations in DNA: MD and crystal structure data analysis. J. Biomol. Struct. Dyn., 23, 13-27.
47. Majumdar, A., Kettani, A., Skripkin, E. and Patel, D.J. (2001) Pulse sequences for detection of NH2. . .N hydrogen bonds in sheared G. A mismatches via remote, non-exchangeable protons. J. Biomol. NMR, 19, 103-113.
48. Cang, X., Šponer, J. and Cheatham, T.E. III (2011) Explaining the varied glycosidic conformational, G-tract length and sequence preferences for anti-parallel G-quadruplexes. Nucleic Acids Res., 39, 4499-4512.
49. Zierkiewicz, W., Michalska, D. and Hobza, P. (2010) Adenine ribbon stabilized by Watson-Crick and Hoogsteen hydrogen bonds: WFT and DFT study. Phys. Chem. Chem. Phys., 12, 2888-2894.
50. Chou, S.H., Zhu, L., Gao, Z., Cheng, J.W. and Reid, B.R. (1996) Hairpin loops consisting of single adenine residues closed by sheared A.A and G.G pairs formed by the DNA triplets AAA and GAG: solution structure of the d(GTACAAAGTAC) hairpin. J. Mol. Biol., 264, 981-1001.
51. Wei, D., Parkinson, G.N., Reszka, A.P. and Neidle, S. (2012) Crystal structure of a c-kit promoter quadruplex reveals the structural role of metal ions and water molecules in maintaining loop conformation. Nucleic Acids Res., 40, 4691-4700.
52. Haider, S., Parkinson, G.N. and Neidle, S. (2002) Crystal structure of the potassium form of an oxytricha nova G-quadruplex. J. Mol. Biol., 320, 189-200.
53. Hainzl, T., Huang, S. and Sauer-Eriksson, A.E. (2002) Structure of the SRP19 RNA complex and implications for signal recognition particle assembly. Nature, 417, 767-771.
54. Juneau, K., Podell, E., Harrington, D.J. and Cech, T.R. (2001) Structural basis of the enhanced stability of a mutant ribozyme domain and a detailed view of RNA-solvent interactions. Structure, 9, 221-231.
55. Zirbel, C.L., Sponer, J.E., Sponer, J., Stombaugh, J. and Leontis, N.B. (2009) Classification and energetics of the base-phosphate interactions in RNA. Nucleic Acids Res., 37, 4898-4918.
56. Carter, A.P., Clemons, W.M., Brodersen, D.E., Morgan- Warren, R.J., Wimberly, B.T. and Ramakrishnan, V. (2000) Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature, 407, 340-348.
57. Webba da Silva, M. (2005) Experimental demonstration of T:(G:G:G:G):T hexad and T:A:A:T tetrad alignments within a DNA quadruplex stem. Biochemistry, 44, 3754-3764.
58. Bazzicalupi, C., Ferraroni, M., Bilia, A.R., Scheggi, F. and Gratteri, P. (2013) The crystal structure of human telomeric DNA complexed with berberine: an interesting case of stacked ligand to G-tetrad ratio higher than 1:1. Nucleic Acids Res., 41, 632-638.
59. Parkinson, G.N., Cuenca, F. and Neidle, S. (2008) Topology conservation and loop flexibility in quadruplex-drug recognition: crystal structures of inter- and intramolecular telomeric DNA quadruplex-drug complexes. J. Mol. Biol., 381, 1145-1156.
60. Sponer, J. and Spackova, N. (2007) Molecular dynamics simulations and their application to four-stranded DNA. Methods, 43, 278-290.
61. Fadrna, E., Spackova, N., Stefl, R., Koca, J., Cheatham, T.E. III and Sponer, J. (2004) Molecular dynamics simulations of Guanine quadruplex loops: advances and force field limitations. Biophys. J., 87, 227-242.
62. Bana s, P., Hollas, D., Zgarbová, M., Jurecka, P., Orozco, M., Cheatham, T.E. III, Šponer, J.i. and Otyepka, M. (2010) Performance of molecular mechanics force fields for RNA simulations: stability of UUCG and GNRA hairpins. J. Chem. Theory Comput., 6, 3836-3849.
63. Kettani, A., Gorin, A., Majumdar, A., Hermann, T., Skripkin, E., Zhao, H., Jones, R. and Patel, D.J. (2000) A dimeric DNA interface stabilized by stacked A.(G.G.G.G).A hexads and coordinated monovalent cations. J. Mol. Biol., 297, 627-644.
64. Abu Almakarem, A.S., Petrov, A.I., Stombaugh, J., Zirbel, C.L. and Leontis, N.B. (2012) Comprehensive survey and geometric classification of base triples in RNA structures. Nucleic Acids Res., 40, 1407-1423.
65. Haider, S.M., Neidle, S. and Parkinson, G.N. (2011) A structural analysis of G-quadruplex/ligand interactions. Biochimie, 93, 1239-1251.
66. Phan, A.T., Kuryavyi, V., Ma, J.B., Faure, A., Andreola, M.L. and Patel, D.J. (2005) An interlocked dimeric parallel-stranded DNA quadruplex: a potent inhibitor of HIV-1 integrase. Proc. Natl Acad. Sci. USA, 102, 634-639.
67. Zhang, N., Gorin, A., Majumdar, A., Kettani, A., Chernichenko, N., Skripkin, E. and Patel, D.J. (2001) V-shaped scaffold: a new architectural motif identified in an A x (G x G x G x G) pentad-containing dimeric DNA quadruplex involving stacked G(anti) x G(anti) x G(anti) x G(syn) tetrads. J. Mol. Biol., 311, 1063-1079.
68. Collie, G.W., Sparapani, S., Parkinson, G.N. and Neidle, S. (2011) Structural basis of telomeric RNA quadruplex-acridine ligand recognition. J. Am. Chem. Soc., 133, 2721-2728.
69. Foloppe, N. and MacKerell, A.D. (1999) Contribution of the phosphodiester backbone and glycosyl linkage intrinsic torsional energetics to DNA structure and dynamics. J. Phys. Chem. B, 103, 10955-10964.
70. Hartmann, B., Piazzola, D. and Lavery, R. (1993) BI - BII transitions in B-DNA. Nucleic Acids Res., 21, 561-568.
71. Hart, K., Foloppe, N., Baker, C.M., Denning, E.J., Nilsson, L. and MacKerell, A.D. (2011) Optimization of the CHARMM additive force field for DNA: improved treatment of the BI/BII conformational equilibrium. J. Chem. Theory Comput., 8, 348-362.
72. Hermann, T. and Patel, D.J. (1999) Stitching together RNA tertiary architectures. J. Mol. Biol., 294, 829-849.