Undulations enhance the effect of helical structure on DNA interactions

Journal of Physical Chemistry B

Volumn 114, Issue 35, 2010, Pages 11668-11680

  Lee, D J ^a,b   Wynveen, A ^c,d   Kornyshev, A A ^a   Leikin, S ^e  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d University of Minnesota   (United States)

^e EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; ALIGNMENT; EXPERIMENTS; GENES; HYDRATES; HYDRATION; MOLECULES; SUGAR (SUCROSE); X RAY DIFFRACTION; X RAY DIFFRACTION ANALYSIS;

CHARGED GROUPS; COUNTERIONS; DNA INTERACTION; DNA SURFACE; DNA-DNA INTERACTION; DOUBLE-HELICAL; HELICAL PATTERN; HELICAL STRUCTURES; NEIGHBORING MOLECULES; OSMOTIC PRESSURE; QUANTITATIVE COMPARISON; STRUCTURAL ADAPTATION; STRUCTURAL DEVIATIONS; SUGAR PHOSPHATE; THERMAL FLUCTUATIONS;

DNA;

EID: 77956322671     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp104552u     Document Type: Article

References (81)

1. Bloomfield, V. A. Curr. Opin. Struct. Biol. 1996, 6, 334
2. Leforestier, A.; Livolant, F. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 9157
3. Tzlil, S.; Kindt, J. T.; Gelbart, W. M.; Ben-Shaul, A. Biophys. J. 2003, 84, 1616
4. Purohit, P. K.; Inamdar, M. M.; Grayson, P. D.; Squires, T. M.; Kondev, J.; Phillips, R. Biophys. J. 2005, 88, 851
5. Gelbart, W. M.; Knobler, C. M. Phys. Today 2008, 61, 42
6. Seeman, N. C.; Lukeman, P. S. Rep. Prog. Phys. 2005, 68, 237
7. Heath, J. R.; Ratner, M. A. Phys. Today 2003, 56, 43
8. Zickler, D. Chromosoma 2006, 115, 158
9. Barzel, A.; Kupiec, M. Nat. Rev. Genet. 2008, 9, 27
10. Baldwin, G. S.; Brooks, N. J.; Robson, R. E.; Wynveen, A.; Goldar, A.; Leikin, S.; Seddon, J. M.; Kornyshev, A. A. J. Phys. Chem. B 2008, 112, 1060
11. Danilowicz, C.; Limouse, C.; Hatch, K.; Conover, A.; Coljee, V. W.; Kleckner, N.; Prentiss, M. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 13196
12. Frank-Kamenetskii, M. D.; Anshelevich, V. V.; Lukashin, A. V. Sov. Phys. Usp. 1987, 151, 595
13. Jayaram, B.; Beveridge, D. L. Annu. Rev. Biophys. Biomol. Struct. 1996, 25, 367
14. Gelbart, W. M.; Bruinsma, R. F.; Pincus, P. A.; Parsegian, V. A. Phys. Today 2000, 53, 38
15. Podgornik, R.; Rau, D. C.; Parsegian, V. A. Biophys. J. 1994, 66, 962
16. Strey, H. H.; Parsegian, V. A.; Podgornik, R. Phys. Rev. E 1999, 59, 999
17. Strey, H. H.; Podgornik, R.; Rau, D. C.; Parsegian, V. A. Curr. Opin. Struct. Biol. 1998, 8, 309
18. Kornyshev, A. A.; Lee, D. J.; Leikin, S.; Wynveen, A. Rev. Mod. Phys. 2007, 79, 943
19. Kandu, M.; Dobnikar, J.; Podgornik, R. Soft Matter 2009, 5, 868
20. Since the interaction of a charge with a dielectric boundary (separating media with different dielectric constants) may be described as it were between the charge and its image(s) across the boundary, this interaction is often referred to as an image force (Landau, L. D.; Lifshitz, E. M. Electrodynamics of continuous media; Pergamon Press: Oxford, U.K., 1982). The force is repulsive when the charge is in a medium with higher dielectric constant and attractive when the charge is in a medium with lower dielectric constant. Image forces have two manifestations in the context of DNA-DNA interactions. First, charges located in water at the surface of one molecule repel from the dielectric core of an opposing molecule. Second, polarization of the dielectric core almost doubles the electric field created in water by a charge located at the core surface, as if the field were created by the charge and its image.
21. Kornyshev, A. A.; Leikin, S. J. Chem. Phys. 1997, 107, 3656
22. Hsiao, C.; Tannenbaum, M.; Van Deusen, H.; Hershkovitz, E.; Perng, G.; Tannenbaum, A.; Williams, L. D. In Nucleic Acid Metal Ion Interactions; Hud, N., Ed.; RSC, London, 2008; pp 1 - 35.
23. Kornyshev, A. A.; Leikin, S. Phys. Rev. Lett. 1999, 82, 4138
24. Kornyshev, A. A.; Leikin, S. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 13579
25. Podgornik, R.; Strey, H. H.; Gawrisch, K.; Rau, D. C.; Rupprecht, A.; Parsegian, V. A. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 4261
26. Kornyshev, A. A.; Leikin, S. Phys. Rev. E 2000, 62, 2576
27. Kornyshev, A. A.; Leikin, S.; Malinin, S. V. Eur. Phys. J. E 2002, 7, 83
28. Cherstvy, A. G. J. Phys. Chem. B 2008, 112, 12585
29. Olson, W. K.; Zhurkin, V. B. Curr. Opin. Struct. Biol. 2000, 10, 286
30. Odijk, T. J. Polym. Sci., Polym. Phys. Ed. 1977, 15, 477
31. Skolnick, J.; Fixman, M. Macromolecules 1977, 10, 945
32. Marko, J. F.; Siggia, E. D. Macromolecules 1995, 28, 8759
33. Cherstvy, A. G.; Kornyshev, A. A.; Leikin, S. J. Phys. Chem. B 2004, 108, 6508
34. Lee, D. J.; Wynveen, A.; Kornyshev, A. A. Phys. Rev. E 2004, 70 051913
35. Lee, D. J.; Wynveen, A. J. Phys.: Condens. Matter 2006, 18, 787
36. Kornyshev, A. A.; Wynveen, A. Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 4683
37. Lee, D. J.; Kornyshev, A. A. J. Chem. Phys. 2009, 131, 155104; Erratum 19901
38. Odijk, T. Biophys. Chem. 1993, 46, 69
39. Smith, D. A. J. Phys. A: Math. Gen. 2001, 34, 4507
40. Podgornik, R.; Parsegian, V. A. Macromolecules 1990, 23, 2265
41. Strey, H. H.; Parsegian, V. A.; Podgornik, R. Phys. Rev. Lett. 1997, 78, 895
42. Selinger, J. V.; Bruinsma, R. F. Phys. Rev. A 1991, 43, 2922
43. Wynveen, A.; Lee, D. J.; Kornyshev, A. A.; Leikin, S. Nucleic Acids Res. 2008, 36, 5540
44. Yakushevich, L. V. Nonlinear Physics of DNA; Wiley: New York, 2004.
45. Bolshoy, A.; McNamara, P.; Harrington, R. E.; Trifonov, E. N. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 2312
46. Koo, H. S.; Wu, H. M.; Crothers, D. M. Nature 1986, 320, 501
47. So far, this approximation has been tested and found valid only for random sequences. (43) It is less clear whether the same approximation also applies to genomic DNA, in which long-range correlations in the base pair composition have been reported (Peng, C.-K.; Buldyrev, C. V.; Goldberger, A. L.; Havlin, S.; Sciortino, F.; Simons, M.; Stanley, H. E. Nature 1992, 356, 168). Potential effects of such correlations in genomic sequences on DNA-DNA interactions are, however, likely to be "washed out" by random juxtaposition of different genomic fragments in fibers.
48. Note that roll, tilt, and slide between adjacent base pairs also depend on the sequence. (29, 45) These lead to small bending distortions, but they do not affect the intrinsic coherence length.
49. Note that each term in eq 5 is a free energy at fixed conformations and separations between the molecules in the aggregate. We refer to these terms as energies to underscore that they do not account for conformational fluctuations of the molecules. For simplicity, eq 5 includes only the energy terms that explicitly depend on the separation and conformation of DNA molecules. Other terms do not have to be explicitly specified in the context of the present theory, but this approach leads to important subtleties in the calculation of derivatives of the aggregate free energy discussed in the Supporting Information.
50. Helfrich, W.; Harbich, W. Chem. Scr. 1985, 25, 32
51. Lee, D. J.; Leikin, S.; Wynveen, A. J. Phys.: Condens. Matter 2010, 22 072202
52. Cherstvy, A. G.; Kornyshev, A. A.; Leikin, S. J. Phys. Chem. B 2002, 106, 13362
53. A variety of theoretical models and computer simulations of counterion-DNA interactions have been reviewed (e.g., Sharp, K. A.; Honig, B. Curr. Opin. Struct. Biol. 1995, 5, 323
54. Beveridge, D. L.; McConnell, K. J. Curr. Opin. Struct. Biol. 2000, 10, 182
55. Cheatham, T. E., III. Curr. Opin. Struct. Biol. 2004, 14, 360
56. Korolev, N.; Lyubartsev, A. P.; Nordenskiöld, L. Adv. Colloid Interface Sci. DOI: 10.1016/j.cis.2009.08.002). However, many of the theoretical predictions are at odds with each other and experiments, which is not surprising given that counterion binding to DNA is strongly affected by the coordination chemistry of the ions, water, and DNA; see, e.g., ref 55. Accurate modeling of such coordination chemistry may require a full quantum mechanical description of electron clouds of all relevant atoms. Furthermore, since counterion binding affects interactions and conformation of DNA in hexagonal aggregates, the converse must also be true; local counterion binding may depend on collective effects concerned with the large scale variations in the DNA interactions and conformation. In other words, modeling of counterion-DNA interactions may require ab initio simulations of millions of interacting atoms over very large time intervals and conformational space, which are still far beyond the reach of the available computational technology.
57. Hud, N., ed. Nucleic Acid Metal Interactions; RSC: London, 2008.
58. Berman, H. M.; Olson, W. K.; Beveridge, D. L.; Westbrook, J.; Gelbin, A.; Demeny, T.; Hsieh, S.-H.; Srinivasan, A. R.; Schneider, B. Biophys. J. 1992, 63, 751
59. b. This suggests that intrinsic bending is not important.
60. Over large length scales, we expect that such effects will not matter.
61. Netz, R. R.; Orland, H. Eur. Phys. J. E 2003, 11, 301
62. Wenner, J. R.; Williams, M. C.; Rouzina, I.; Bloomfield, V. A. Biophys. J. 2002, 82, 3160
63. Crothers, D. M.; Drak, J.; Kahn, J. D.; Levene, S. D. Methods Enzymol. 1992, 212, 3
64. Note that this model formally allows unrestricted thermal undulations, resulting in nonphysical overlap between the cores of the molecules. Although the probability of such overlap is low, this feature of the model requires some caution in averaging of the electrostatic energy (see the Supporting Information).
65. Bogoliubov, N. N. Dokl. Akad. Nauk SSSR 1958, 119, 244
66. Rau, D. C.; Lee, B.; Parsegian, V. A. Proc. Natl. Acad. Sci. U.S.A. 1984, 81, 2621
67. Rau, D. C.; Parsegian, V. A. Biophys. J. 1992, 61, 246
68. Rau, D. C.; Parsegian, V. A. Biophys. J. 1992, 61, 260.
69. Todd, B. A.; Parsegian, V. A.; Shirahata, A.; Thomas, T. J.; Rau, D. C. Biophys. J. 2008, 94, 4775
70. Odijk, T. Macromolecules 1983, 16, 1340
71. B as the deflection length.
72. Harreis, H. M.; Kornyshev, A. A.; Likos, C. N.; Löwen, H.; Sutmann, G. Phys. Rev. Lett. 2002, 89 018303
73. Wynveen, A.; Lee, D. J.; Kornyshev, A. A. Eur. Phys. J. E 2005, 16, 303
74. We neglect the weak attraction resulting from correlated thermal fluctuations of the helical phase of neighbor molecules, (35, 70) which is akin to and should be considered together with the zero-frequency van der Waals attraction.
75. 2 as adjustable parameters may result in overfitting the data.
76. Saenger, W. Principles of Nucleic Acid Structure; Springer: New York, 1983.
77. Wemmer, D. E.; Srivenugopal, K. S.; Reid, B. R.; Morris, D. R. J. Mol. Biol. 1985, 185, 457
78. Yang, J.; Rau, D. C. Biophys. J. 2005, 89, 1932
79. Livolant, F.; Leforestier, A. Prog. Polym. Sci. 1996, 21, 1115
80. Kornyshev, A. A.; Lee, D. J.; Leikin, S.; Wynveen, A.; Zimmerman, S. B. Phys. Rev. Lett. 2005, 95, 148102
81. Mar-elja, S.; Radic, N. Chem. Phys. Lett. 1976, 42, 129