Bulletin of the Korean Chemical Society

Korean Chemical Society (대한화학회)
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Contribution of Counterion Entropy to the Salt-Induced Transition Between B-DNA and Z-DNA

  • Lee, Youn-Kyoung (Department of Chemistry, Seoul National University) ;
  • Lee, Juyong (Department of Chemistry, Seoul National University) ;
  • Choi, Jung Hyun (Department of Chemistry, Seoul National University) ;
  • Seok, Chaok (Department of Chemistry, Seoul National University)
  • Received : 2012.08.11
  • Accepted : 2012.08.14
  • Published : 2012.11.20
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Abstract

Formation of Z-DNA, a left-handed double helix, from B-DNA, the canonical right-handed double helix, occurs during important biological processes such as gene expression and DNA transcription. Such B-Z transitions can also be induced by high salt concentration in vitro, but the changes in the relative stability of B-DNA and Z-DNA with salt concentration have not been fully explained despite numerous attempts. For example, electrostatic effects alone could not account for salt-induced B-Z transitions in previous studies. In this paper, we propose that the B-Z transition can be explained if counterion entropy is considered along with the electrostatic interactions. This can be achieved by conducting all-atom, explicit-solvent MD simulations followed by MM-PBSA and molecular DFT calculations. Our MD simulations show that counterions tend to bind at specific sites in B-DNA and Z-DNA, and that more ions cluster near Z-DNA than near B-DNA. Moreover, the difference in counterion ordering near B-DNA and Z-DNA is larger at a low salt concentration than at a high concentration. The results imply that the exclusion of counterions by Z-DNA-binding proteins may facilitate Z-DNA formation under physiological conditions.

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References

  1. Rich, A.; Nordheim, A.; Wang, A. Annual Review of Biochemistry 1984, 53, 791. https://doi.org/10.1146/annurev.bi.53.070184.004043
  2. Rich, A.; Zhang, S. Nature Reviews Genetics 2003, 4, 566.
  3. Wittig, B.; Dorbic, T.; Rich, A. Proceedings of the National Academy of Sciences of the United States of America 1991, 88, 2259. https://doi.org/10.1073/pnas.88.6.2259
  4. Rahmouni, A.; Wells, R. Science 1989, 246, 358. https://doi.org/10.1126/science.2678475
  5. Takaoka, A.; Wang, Z.; Choi, M.; Yanai, H.; Negishi, H.; Ban, T.; Lu, Y.; Miyagishi, M.; Kodama, T.; Honda, K. Nature 2007, 448, 501. https://doi.org/10.1038/nature06013
  6. Boehm, T.; Mengle-Gaw, L.; Kees, U.; Spurr, N.; Lavenir, I.; Forster, A.; Rabbitts, T. The EMBO Journal 1989, 8, 2621.
  7. Thandla, S.; Ploski, J.; Raza-Egilmez, S.; Chhalliyil, P.; Block, A.; de Jong, P.; Aplan, P. Blood 1999, 93, 293.
  8. Wang, G.; Christensen, L.; Vasquez, K. Proceedings of the National Academy of Sciences 2006, 103, 2677. https://doi.org/10.1073/pnas.0511084103
  9. Behe, M.; Felsenfeld, G. Proceedings of the National Academy of Sciences of the United States of America 1981, 78, 1619. https://doi.org/10.1073/pnas.78.3.1619
  10. Ramstein, J.; Leng, M. Nature 1980, 288, 413. https://doi.org/10.1038/288413a0
  11. Maruyama, Y.; Yoshida, N.; Hirata, F. J. Phys. Chem. B 2010, 375.
  12. Klement, R.; Soumpasis, D.; Kitzing, E.; Jovin, T. Biopolymers 2004, 29, 1089.
  13. Kollman, P.; Weiner, P.; Quigley, G.; Wang, A. Biopolymers 1982, 21, 1945. https://doi.org/10.1002/bip.360211003
  14. Matthew, J.; Richards, F. Biopolymers 1984, 23, 2743. https://doi.org/10.1002/bip.360231205
  15. Gueron, M.; Demaret, J. Proceedings of the National Academy of Sciences 1992, 89, 5740. https://doi.org/10.1073/pnas.89.13.5740
  16. Gueron, M.; Demaret, J.; Filoche, M. Biophysical Journal 2000, 78, 1070. https://doi.org/10.1016/S0006-3495(00)76665-3
  17. Wereszczynski, J.; Andricioaei, I. J. Phys. Chem. B 2010, 62.
  18. Ponomarev, S.; Thayer, K.; Beveridge, D. Proceedings of the National Academy of Sciences of the United States of America 2004, 101, 14771. https://doi.org/10.1073/pnas.0406435101
  19. Misra, V.; Honig, B. Biochemistry 1996, 35, 1115. https://doi.org/10.1021/bi951463y
  20. Tashiro, R.; Sugiyama, H. Angewandte Chemie 2003, 115, 6200. https://doi.org/10.1002/ange.200352752
  21. Behe, M.; Felsenfeld, G.; Szu, S.; Charney, E. Biopolymers 2004, 24, 289.
  22. Holak, T.; Borer, P.; Levy, G.; Van Boom, J.; Wang, A. Nucleic Acids Research 1984, 12, 4625. https://doi.org/10.1093/nar/12.11.4625
  23. Hud, N.; Polak, M. Current Opinion in Structural Biology 2001, 11, 293. https://doi.org/10.1016/S0959-440X(00)00205-0
  24. Howerton, S.; Sines, C.; VanDerveer, D.; Williams, L. Biochemistry 2001, 40, 10023. https://doi.org/10.1021/bi010391+
  25. Gavryushov, S.; Zielenkiewicz, P. Biophysical Journal 1998, 75, 2732. https://doi.org/10.1016/S0006-3495(98)77717-3
  26. Grochowski, P.; Trylska, J. Peptide Science 2008, 89, 93. https://doi.org/10.1002/bip.20877
  27. Dong, F.; Wagoner, J.; Baker, N. Physical Chemistry Chemical Physics: PCCP 2008, 10, 4889. https://doi.org/10.1039/b807384h
  28. Bansal, M.; Bhattacharyya, D.; Ravi, B. Bioinformatics 1995, 11, 281. https://doi.org/10.1093/bioinformatics/11.3.281
  29. Wang, A.; Quigley, G.; Kolpak, F.; Van der Marel, G.; Van Boom, J.; Rich, A. Science 1981, 211, 171. https://doi.org/10.1126/science.7444458
  30. Case, D. A.; Darden, T. A.; Cheatham, T. E., III; Simmerling, C. L.; Wang, J.; Duke, R. E.; Luo, R.; Crowley, M.; Walker, R. C.; Zhang, W.; Merz, K. M.; Wang, B.; Hayik, S.; Roitberg, A.; Seabra, G.; Kolossváry, I.; Wong, K. F.; Paesani, F.; Vanicek, J.; Wu, X.; Brozell, S. R.; Steinbrecher, T.; Gohlke, H.; Yang, L.; Tan, C.; Mongan, J.; Hornak, V.; Cui, G.; Mathews, D. H.; Seetin, M. G.; Sagui, C.; Babin, V.; Kollman, P. A. AMBER10; University of California, San Francisco, 2008.
  31. Perez, A.; Marchan, I.; Svozil, D.; Sponer, J.; Cheatham, T.; Laughton, C.; Orozco, M. Biophysical Journal 2007, 92, 3817. https://doi.org/10.1529/biophysj.106.097782
  32. Joung, I.; Cheatham, T. J. Phys. Chem. B 2008, 112, 9020. https://doi.org/10.1021/jp8001614
  33. Darden, T.; York, D.; Pedersen, L. J. Chem. Phys. 1993, 98, 10089. https://doi.org/10.1063/1.464397
  34. Berendsen, H.; Postma, J.; Van Gunsteren, W.; DiNola, A.; Haak, J. J. Chem. Phys. 1984, 81, 3684. https://doi.org/10.1063/1.448118
  35. Lavery, R.; Moakher, M.; Maddocks, J.; Petkeviciute, D.; Zakrzewska, K. Nucleic Acids Research 2009.
  36. Luo, R.; David, L.; Gilson, M. Journal of Computational Chemistry 2002, 23, 1244. https://doi.org/10.1002/jcc.10120
  37. Sitkoff, D.; Sharp, K.; Honig, B. J. Phys. Chem. 1994, 98, 1978. https://doi.org/10.1021/j100058a043
  38. Oxtoby, D. W.; Evans, R. J. Chem. Phys. 1988, 7521.
  39. Seok, C.; Oxtoby, D. W. J. Chem. Phys. 1998, 7982.
  40. Oxtoby, D. W. Crystallization of Liquids: A Density Functional Approach Liquids Freezing and Glass Transition, 1990.
  41. Perez, A.; Lankas, F.; Luque, F.; Orozco, M. Nucleic Acids Research 2008, 36, 2379. https://doi.org/10.1093/nar/gkn082
  42. Thomas, T.; Bloomfield, V. Nucleic Acids Research 1983, 11, 1919. https://doi.org/10.1093/nar/11.6.1919
  43. Duchardt, E.; Nilsson, L.; Schleucher, J. Nucleic Acids Research 2008, 36, 4211. https://doi.org/10.1093/nar/gkn375
  44. Irikura, K.; Tidor, B.; Brooks, B.; Karplus, M. Science 1985, 229, 571. https://doi.org/10.1126/science.3839596
  45. Escudero, D.; Estarellas, C.; Frontera, A.; Quinonero, D.; Deya, P. Chem. Phys. Lett. 2009.
  46. Egli, M.; Gessner, R. Proceedings of the National Academy of Sciences of the United States of America 1995, 92, 180. https://doi.org/10.1073/pnas.92.1.180
  47. Sponer, J.; Gabb, H.; Leszczynski, J.; Hobza, P. Biophysical Journal 1997, 73, 76. https://doi.org/10.1016/S0006-3495(97)78049-4
  48. Chaires, J.; Sturtevant, J. Biopolymers 1988, 27, 1375. https://doi.org/10.1002/bip.360270905

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