All-atomic simulations on human telomeric G-quadruplex DNA binding with thioflavin T

Journal of Physical Chemistry B

Volumn 119, Issue 15, 2015, Pages 4955-4967

  Luo, Di ^a   Mu, Yuguang ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BIOINFORMATICS; CONFORMATIONS; DNA; DNA SEQUENCES; FREE ENERGY; LIGANDS; MOLECULAR DYNAMICS;

ANTI-CANCER AGENTS; ATOMIC SIMULATIONS; BINDING AFFINITIES; BINDING BEHAVIORS; BINDING MECHANISMS; CONFORMATIONAL CHANGE; FREE ENERGY LANDSCAPE; LIGAND-STABILIZED;

BINDING ENERGY;

DNA; GUANINE QUADRUPLEX; POTASSIUM; SODIUM; THIAZOLE DERIVATIVE; THIOFLAVINE;

BIOLOGICAL MODEL; CHEMISTRY; COMPUTER SIMULATION; HUMAN; HYDROGEN BOND; MOLECULAR DYNAMICS; TELOMERE;

COMPUTER SIMULATION; DNA; G-QUADRUPLEXES; HUMANS; HYDROGEN BONDING; MODELS, GENETIC; MOLECULAR DYNAMICS SIMULATION; POTASSIUM; SODIUM; TELOMERE; THIAZOLES;

EID: 84928041686     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b01107     Document Type: Article

References (59)

1. Simonsson, T. G-Quadruplex DNA Structures-Variations on a Theme Biol. Chem. 2001, 382, 621-628
2. Todd, A. K.; Johnston, M.; Neidle, S. Highly Prevalent Putative Quadruplex Sequence Motifs in Human DNA Nucleic Acids Res. 2005, 33, 2901-2907
3. Tarsounas, M.; Tijsterman, M. Genomes and G-Quadruplexes: For Better or for Worse J. Mol. Biol. 2013, 425, 4782-4789
4. Paeschke, K.; Capra, J. A.; Zakian, V. A. DNA Replication through G-Quadruplex Motifs Is Promoted by the Saccharomyces Cerevisiae Pif1 DNA Helicase Cell 2011, 145, 678-691
5. Sarkies, P.; Murat, P.; Phillips, L. G.; Patel, K. J.; Balasubramanian, S.; Sale, J. E. Fancj Coordinates Two Pathways That Maintain Epigenetic Stability at G-Quadruplex DNA Nucleic Acids Res. 2012, 40, 1485-1498
6. Moyzis, R. K.; Buckingham, J. M.; Cram, L. S.; Dani, M.; Deaven, L. L.; Jones, M. D.; Meyne, J.; Ratliff, R. L.; Wu, J. R. A Highly Conserved Repetitive DNA-Sequence, (TTAGGG)n, Present at the Telomeres of Human-Chromosomes Proc. Natl. Acad. Sci. U. S. A. 1988, 85, 6622-6626
7. Parkinson, G. N.; Lee, M. P. H.; Neidle, S. Crystal Structure of Parallel Quadruplexes from Human Telomeric DNA Nature 2002, 417, 876-880
8. 3] G-Tetraplex Structure 1993, 1, 263-282
9. + Solution Nucleic Acids Res. 2007, 35, 6517-6525
10. + Solution: A Stable Basket-Type G-Quadruplex with Only Two G-Tetrad Layers J. Am. Chem. Soc. 2009, 131, 4301-4309
11. Biffi, G.; Tannahill, D.; McCafferty, J.; Balasubramanian, S. Quantitative Visualization of DNA G-Quadruplex Structures in Human Cells Nat. Chem. 2013, 5, 182-186
12. Harley, C. B.; Futcher, A. B.; Greider, C. W. Telomeres Shorten During Aging of Human Fibroblasts Nature 1990, 345, 458-460
13. Bodnar, A. G.; Ouellette, M.; Frolkis, M.; Holt, S. E.; Chiu, C. P.; Morin, G. B.; Harley, C. B.; Shay, J. W.; Lichtsteiner, S.; Wright, W. E. Extension of Life-Span by Introduction of Telomerase into Normal Human Cells Science 1998, 279, 349-352
14. Counter, C. M.; Avilion, A. A.; Lefeuvre, C. E.; Stewart, N. G.; Greider, C. W.; Harley, C. B.; Bacchetti, S. Telomere Shortening Associated with Chromosome Instability Is Arrested in Immortal Cells Which Express Telomerase Activity EMBO J. 1992, 11, 1921-1929
15. Feng, J. L.; Funk, W. D.; Wang, S. S.; Weinrich, S. L.; Avilion, A. A.; Chiu, C. P.; Adams, R. R.; Chang, E.; Allsopp, R. C.; Yu, J. H. The RNA Component of Human Telomerase Science 1995, 269, 1236-1241
16. Zahler, A. M.; Williamson, J. R.; Cech, T. R.; Prescott, D. M. Inhibition of Telomerase by G-Quartet DNA Structures Nature 1991, 350, 718-720
17. Sun, D. Y.; Thompson, B.; Cathers, B. E.; Salazar, M.; Kerwin, S. M.; Trent, J. O.; Jenkins, T. C.; Neidle, S.; Hurley, L. H. Inhibition of Human Telomerase by a G-Quadruplex-Interactive Compound J. Med. Chem. 1997, 40, 2113-2116
18. Mergny, J. L.; Helene, C. G-Quadruplex DNA: A Target for Drug Design Nat. Med. 1998, 4, 1366-1367
19. Kim, M. Y.; Vankayalapati, H.; Kazuo, S.; Wierzba, K.; Hurley, L. H. Telomestatin, a Potent Telomerase Inhibitor That Interacts Quite Specifically with the Human Telomeric Intramolecular G-Quadruplex J. Am. Chem. Soc. 2002, 124, 2098-2099
20. Haudecoeur, R.; Stefan, L.; Denat, F.; Monchaud, D. A Model of Smart G-Quadruplex Ligand J. Am. Chem. Soc. 2013, 135, 550-553
21. Dixon, I. M.; Lopez, F.; Tejera, A. M.; Esteve, J. P.; Blasco, M. A.; Pratviel, G.; Meunier, B. A G-Quadruplex Ligand with 10000-Fold Selectivity over Duplex DNA J. Am. Chem. Soc. 2007, 129, 1502-1503
22. Rodriguez, R.; Pantos, G. D.; Goncalves, D. P. N.; Sanders, J. K. M.; Balasubramanian, S. Ligand-Driven G-Quadruplex Conformational Switching by Using an Unusual Mode of Interaction Angew. Chem., Int. Ed. 2007, 46, 5405-5407
23. Campbell, N. H.; Patel, M.; Tofa, A. B.; Ghosh, R.; Parkinson, G. N.; Neidle, S. Selectivity in Ligand Recognition of G-Quadruplex Loops Biochemistry 2009, 48, 1675-1680
24. Haider, S. M.; Parkinson, G. N.; Neidle, S. Structure of a G-Quadruplex-Ligand Complex J. Mol. Biol. 2003, 326, 117-125
25. Campbell, N. H.; Smith, D. L.; Reszka, A. P.; Neidle, S.; O'Hagan, D. Fluorine in Medicinal Chemistry: Beta-Fluorination of Peripheral Pyrrolidines Attached to Acridine Ligands Affects Their Interactions with G-Quadruplex DNA Org. Biomol. Chem. 2011, 9, 1328-1331
26. Collie, G. W.; Promontorio, R.; Hampel, S. M.; Micco, M.; Neidle, S.; Parkinson, G. N. Structural Basis for Telomeric G-Quadruplex Targeting by Naphthalene Diimide Ligands J. Am. Chem. Soc. 2012, 134, 2723-2731
27. Micco, M.; Collie, G. W.; Dale, A. G.; Ohnmacht, S. A.; Pazitna, I.; Gunaratnam, M.; Reszka, A. P.; Neidle, S. Structure-Based Design and Evaluation of Naphthalene Diimide G-Quadruplex Ligands as Telomere Targeting Agents in Pancreatic Cancer Cells J. Med. Chem. 2013, 56, 2959-2974
28. Wilson, T.; Costa, P. J.; Felix, V.; Williamson, M. P.; Thomas, J. A. Structural Studies on Dinuclear Ruthenium(II) Complexes That Bind Diastereoselectively to an Antiparallel Folded Human Telomere Sequence J. Med. Chem. 2013, 56, 8674-8683
29. Read, M. A.; Neidle, S. Structural Characterization of a Guanine-Quadruplex Ligand Complex Biochemistry 2000, 39, 13422-13432
30. Corry, B.; Smith, N. M. The Role of Thermodynamics and Kinetics in Ligand Binding to G-Quadruplex DNA Chem. Commun. 2012, 48, 8958-8960
31. Di Leva, F. S.; Novellino, E.; Cavalli, A.; Parrinello, M.; Limongelli, V. Mechanistic Insight into Ligand Binding to G-Quadruplex DNA Nucleic Acids Res. 2014, 42, 5447-5455
32. Hou, J. Q.; Chen, S. B.; Tan, J. H.; Luo, H. B.; Li, D.; Gu, L. Q.; Huang, Z. S. New Insights from Molecular Dynamic Simulation Studies of the Multiple Binding Modes of a Ligand with G-Quadruplex DNA J. Comput.-Aided Mol. Des. 2012, 26, 1355-1368
33. Husby, J.; Todd, A. K.; Platts, J. A.; Neidle, S. Small-Molecule G-Quadruplex Interactions: Systematic Exploration of Conformational Space Using Multiple Molecular Dynamics Biopolymers 2013, 99, 989-1005
34. Li, A. X.; Maurel, F.; Barbault, F.; Delamar, M.; Wang, B. S.; Zhou, X.; Wang, P. Molecular Modeling Study of Binding Site Selectivity of Tqmp to G-Quadruplex DNA Eur. J. Med. Chem. 2010, 45, 983-991
35. Gabelica, V.; Maeda, R.; Fujimoto, T.; Yaku, H.; Murashima, T.; Sugimoto, N.; Miyoshi, D. Multiple and Cooperative Binding of Fluorescence Light-up Probe Thioflavin T with Human Telomere DNA G-Quadruplex Biochemistry 2013, 52, 5620-5628
36. Mohanty, J.; Barooah, N.; Dhamodharan, V.; Harikrishna, S.; Pradeepkumar, P. I.; Bhasikuttan, A. C. Thioflavin T as an Efficient Inducer and Selective Fluorescent Sensor for the Human Telomeric G-Quadruplex DNA J. Am. Chem. Soc. 2013, 135, 367-376
37. de la Faverie, A. R.; Guedin, A.; Bedrat, A.; Yatsunyk, L. A.; Mergny, J. L. Thioflavin T as a Fluorescence Light-up Probe for G4 Formation Nucleic Acids Res. 2014, 42, e65
38. + Sensor Anal. Chem. 2014, 86, 1622-1631
39. Barducci, A.; Bussi, G.; Parrinello, M. Well-Tempered Metadynamics: A Smoothly Converging and Tunable Free-Energy Method Phys. Rev. Lett. 2008, 100, 020603
40. Laio, A.; Gervasio, F. L. Metadynamics: A Method to Simulate Rare Events and Reconstruct the Free Energy in Biophysics, Chemistry and Material Science Rep. Prog. Phys. 2008, 71, 126601
41. Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T. E.; Laughton, C. A.; Orozco, M. Refinement of the Amber Force Field for Nucleic Acids: Improving the Description of Alpha/Gamma Conformers Biophys. J. 2007, 92, 3817-3829
42. Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.; Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Scalmani, G.; Barone, V.; Mennucci, B.; Petersson, G. A.; Gaussian 09; Gaussian, Inc.: Wallingford, CT, USA, 2009.
43. Bayly, C. I.; Cieplak, P.; Cornell, W. D.; Kollman, P. A. A Well-Behaved Electrostatic Potential Based Method Using Charge Restraints for Deriving Atomic Charges: the RESP Model J. Phys. Chem. 1993, 97, 10269-10280
44. Wang, J. M.; Wang, W.; Kollman, P. A. Antechamber: An Accessory Software Package for Molecular Mechanical Calculations. Abstracts of Papers, 222nd National Meeting of the American Chemical Society, Chicago, IL, Aug 26-30, 2001; American Chemical Society: Washington, DC, 2001; U403.
45. Wang, J. M.; Wolf, R. M.; Caldwell, J. W.; Kollman, P. A.; Case, D. A. Development and Testing of a General Amber Force Field J. Comput. Chem. 2004, 25, 1157-1174
46. 2+ Ions for All-Atom Molecular Dynamics Simulations of Nucleic Acid Systems J. Phys. Chem. Lett. 2012, 3, 45-50
47. Darden, T.; York, D.; Pedersen, L. Particle Mesh Ewald: an N∗Log(N) Method for Ewald Sums in Large Systems J. Chem. Phys. 1993, 98, 10089-10092
48. Hess, B. P-LINCS: A Parallel Linear Constraint Solver for Molecular Simulation J. Chem. Theory Comput. 2008, 4, 116-122
49. Bussi, G.; Donadio, D.; Parrinello, M. Canonical Sampling through Velocity Rescaling J. Chem. Phys. 2007, 126, 014101
50. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. Gromacs 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447
51. Daura, X.; Gademann, K.; Jaun, B.; Seebach, D.; van Gunsteren, W. F.; Mark, A. E. Peptide Folding: When Simulation Meets Experiment Angew. Chem., Int. Ed. 1999, 38, 236-240
52. Srinivasan, J.; Cheatham, T. E.; Cieplak, P.; Kollman, P. A.; Case, D. A. Continuum Solvent Studies of the Stability of DNA, RNA, and Phosphoramidate-DNA Helices J. Am. Chem. Soc. 1998, 120, 9401-9409
53. Kollman, P. A.; Massova, I.; Reyes, C.; Kuhn, B.; Huo, S. H.; Chong, L.; Lee, M.; Lee, T.; Duan, Y.; Wang, W. Calculating Structures and Free Energies of Complex Molecules: Combining Molecular Mechanics and Continuum Models Acc. Chem. Res. 2000, 33, 889-897
54. Kirkwood, J. G. Statistical Mechanics of Fluid Mixtures J. Chem. Phys. 1935, 3, 300-313
55. Zwanzig, R. W. High-Temperature Equation of State by a Perturbation Method. I. Nonpolar Gases J. Chem. Phys. 1954, 22, 1420-1426
56. Hunter, C. A.; Sanders, J. K. M. The Nature of Pi-Pi Interactions J. Am. Chem. Soc. 1990, 112, 5525-5534
57. Bazzicalupi, C.; Ferraroni, M.; Bilia, A. R.; Scheggi, F.; Gratteri, P. 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. 2013, 41, 632-638
58. Plevin, M. J.; Bryce, D. L.; Boisbouvier, J. Direct Detection of CH/Pi Interactions in Proteins Nat. Chem. 2010, 2, 466-471
59. Mcghee, J. D.; Hippel, P. H. V. Theoretical Aspects of DNA-Protein Interactions: Cooperative and Non-Cooperative Binding of Large Ligands to a One-Dimensional Homogeneous Lattice J. Mol. Biol. 1974, 86, 469-489