Structural, mechanical, and thermodynamic properties of a coarse-grained DNA model

Journal of Chemical Physics

Volumn 134, Issue 8, 2011, Pages

  Ouldridge, Thomas E ^a   Louis, Ard A ^a   Doye, Jonathan P K ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BASE STACKING; CHAIN CONNECTIVITY; COARSE GRAINED MODELS; COARSE-GRAINED; DNA MODEL; DOUBLE HELIX; DUPLEX FORMATION; EFFECTIVE INTERACTIONS; EXCLUDED VOLUME; HAIRPIN FORMATION; HYDROGEN BONDINGS; INTERACTION STRENGTH; INTERNAL LOOPS; NANOTWEEZERS; PERSISTENCE LENGTH; WATSON-CRICK BASE PAIRING;

DNA; ELASTIC MODULI; HYDROGEN BONDS; MECHANICAL PROPERTIES; THERMODYNAMIC PROPERTIES;

NUCLEIC ACIDS;

DNA;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; MECHANICS; THERMODYNAMICS;

DNA; MECHANICAL PHENOMENA; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; THERMODYNAMICS;

EID: 79952091255     PISSN: 00219606     EISSN: None     Source Type: Journal    
DOI: 10.1063/1.3552946     Document Type: Article

References (120)

1. W. Saenger, Principles of Nucleic Acid Structure (Springer-Verlag, New York, 1984).
2. J. D. Watson and F. H.C. Crick, Nature (London) 171, 737 (1953). 10.1038/171737a0
3. P. J. Hagerman, Annu. Rev. Biophys. Biophys. Chem. 17, 265 (1988). 10.1146/annurev.bb.17.060188.001405
4. N. R. Kallenbach, R.-I. Ma, and N. C. Seeman, Nature (London) 305, 829 (1983). 10.1038/305829a0
5. T. J. Fu and N. C. Seeman, Biochemistry 32, 3211 (1993). 10.1021/bi00064a003
6. H. Yan, S. H. Park, G. Finkelstein, J. H. Reif, and T. H. LaBean, Science 301, 1882 (2003). 10.1126/science.1089389 (Pubitemid 37221388)
7. E. Winfree, F. R. Liu, L. A. Wenzler, and N. C. Seeman, Nature (London) 394, 539 (1998). 10.1038/28998 (Pubitemid 28366820)
8. J. Malo, J. C. Mitchell, C. Venien-Bryan, J. R. Harris, H. Wille, D. J. Sherrat, and A. J. Turberfield, Angew. Chem., Int. Ed. 44, 3057 (2005). 10.1002/anie.200463027 (Pubitemid 40689844)
9. J. Chen and N. C. Seeman, Nature (London) 350, 631 (1991). 10.1038/350631a0
10. Y. Zhang and N. C. Seeman, J. Am. Chem. Soc. 116, 1661 (1994). 10.1021/ja00084a006
11. R. P. Goodman, I. A.T. Sharp, C. F. Tardin, C. M. Erben, R. M. Berry, C. F. Schmidt, and A. J. Turberfield, Science 310, 1661 (2005). 10.1126/science.1120367 (Pubitemid 41780784)
12. C. M. Erben, R. P. Goodman, and A. J. Turberfield, J. Am. Chem. Soc. 129, 6992 (2007). 10.1021/ja071493b (Pubitemid 46903253)
13. W. M. Shih, J. D. Quispe, and G. F. Joyce, Nature (London) 427, 618 (2004). 10.1038/nature02307 (Pubitemid 38248477)
14. F. F. Andersen, B. Knudsen, C. L.P. Oliveira, R. F. Frohlich, D. Kruger, J. Bungert, M. Agbandje-McKenna, R. McKenna, S. Juul, C. Veigaard, J. Koch, J. L. Rubinstein, B. Guldbrandtsen, M. S. Hede, G. Karlsson, A. H. Andersen, J. S. Pedersen, and B. R. Knudsen, Nucleic Acids Res. 36, 1113 (2008). 10.1093/nar/gkm1124 (Pubitemid 351330929)
15. Y. He, T. Ye, M. Su, C. Zhang, A. Ribbe, W. Jiang, and C. Mao, Nature (London) 452, 198 (2008). 10.1038/nature06597 (Pubitemid 351380239)
16. P. W.K. Rothemund, Nature (London) 440, 297 (2006). 10.1038/nature04586
17. E. S. Andersen, M. Dong, M. M. Nielsen, K. Jahn, R. Subramani, W. Mamdouh, M. M. Golas, B. Sander, H. Stark, C. L.P. Oliveira, J. S. Pedersen, V. Birkedal, F. Besenbacher, K. V. Gothelf, and J. Kjems, Nature (London) 459, 73 (2009). 10.1038/nature07971
18. S. M. Douglas, H. Dietz, T. Liedl, B. Hgberg, F. Graf, and W. M. Shih, Nature (London) 459, 414 (2009). 10.1038/nature08016
19. Z. Li, B. Wei, J. Nangreave, C. Lin, Y. Liu, Y. Mi, and H. Yan, J. Am. Chem. Soc. 131, 13093 (2009). 10.1021/ja903768f
20. F. A. Aldaye and H. F. Sleiman, J. Am. Chem. Soc. 129, 13376 (2007). 10.1021/ja075966q (Pubitemid 350071751)
21. J. Zimmermann, M. P. Cebulla, S. Monninghoff, and G. von Kiedrowski, Angew. Chem., Int. Ed. 47, 3626 (2008). 10.1002/anie.200702682
22. J. Bath and A. J. Turberfield, Nat. Nanotechnol. 2, 275 (2007). 10.1038/nnano.2007.104 (Pubitemid 46882966)
23. B. Yurke, A. J. Turberfield, A. P. Mills, F. C. Simmel, and J. Neumann, Nature (London) 406, 605 (2000). 10.1038/35020524 (Pubitemid 30641042)
24. W. B. Sherman and N. C. Seeman, Nano Lett. 4, 1203 (2004). 10.1021/nl049527q (Pubitemid 39092159)
25. J.-S. Shin and N. A. Pierce, J. Am. Chem. Soc. 126, 10834 (2004). 10.1021/ja047543j (Pubitemid 39180556)
26. J. Bath, S. J. Green, K. E. Allan, and A. J. Turberfield, Small 5, 1513 (2009). 10.1002/smll.200900078
27. S. J. Green, J. Bath, and A. J. Turberfield, Phys. Rev. Lett. 101, 238101 (2008). 10.1103/PhysRevLett.101.238101
28. C. Zhang, J. Yang, and J. Xu, Langmuir 26, 1416 (2010). 10.1021/la903137f
29. T. Liedl and F. C. Simmel, Nano Lett. 5, 1894 (2005). 10.1021/nl051180j (Pubitemid 41546310)
30. R. R. Sinden, DNA Structure and Function (Academic, London, 1994).
31. M. Orozco, A. Pérez, A. Noy, and F. J. Luque, Chem. Soc. Rev. 32, 350 (2003). 10.1039/b207226m
32. R. Lavery, K. Zakrzewska, D. Beveridge, T. C. Bishop, D. A. Case, T. Cheetham III, S. Dixit, B. Jayaram, F. Lankas, C. Laughton, J. H. Maddocks, A. Michon, R. Osman, M. Orozco, A. Perez, T. Singh, N. Spackova, and J. Sponer, Nucleic Acids Res. 38, 299 (2010). 10.1093/nar/gkp834
33. A. Pérez, F. J. Luque, and M. Orozco, J. Am. Chem. Soc. 129, 14739 (2007). 10.1021/ja0753546 (Pubitemid 350207887)
34. C. Mura and A. J. McCammon, Nucleic Acids Res. 36, 4941 (2008). 10.1093/nar/gkn473
35. S. Kannan and M. Zacharias, Phys. Chem. Chem. Phys. 11, 10589 (2009). 10.1039/b910792b
36. E. J. Sorin, Y. M. Rhee, B. J. Nakatani, and V. S. Pande, Biophys. J. 85, 790 (2003). 10.1016/S0006-3495(03)74520-2
37. S. Kannan and M. Zacharias, Biophys. J. 93, 3218 (2007). 10.1529/biophysj.107.108019 (Pubitemid 350097112)
38. D. Swigon, Mathematics of DNA Structure, Function and Interactions (Springer, New York, 2009), Chap. XIII, pp. 293-320.
39. S. Khalid, P. J. Bond, J. Holyoake, R. W. Hawtin, and M. S. Sansom, J. R. Soc., Interface 5, 241 (2008). 10.1098/rsif.2008.0239.focus
40. J. Corsi, R. W. Hawtin, O. Ces, G. S. Attard, and S. Khalid, Langmuir 26, 12119 (2010). 10.1021/la101448m
41. D. Poland and H. A. Scheraga, J. Chem. Phys. 45, 1464 (1966). 10.1063/1.1727786
42. J. SantaLucia Jr., Proc. Natl. Acad. Sci. U.S.A. 17, 1460 (1998). 10.1073/pnas.95.4.1460 (Pubitemid 28103414)
43. J. SantaLucia Jr. and D. Hicks, Annu. Rev. Biophys. Biomol. Struct. 33, 415 (2004). 10.1146/annurev.biophys.32.110601.141800 (Pubitemid 38829966)
44. R. Everaers, S. Kumar, and C. Simm, Phys. Rev. E 75, 041918 (2007). 10.1103/PhysRevE.75.041918 (Pubitemid 46677018)
45. T. Dauxois, M. Peyrard, and A. R. Bishop, Phys. Rev. E 47, 684 (1993). 10.1103/PhysRevE.47.684
46. N. B. Becker and R. Everaers, J. Chem. Phys. 130, 135102 (2009). 10.1063/1.3082157
47. F. Lanka, O. Gonzalez, L. M. Heffler, G. Stoll, M. Moakher, and J. H. Maddocks, Phys. Chem. Chem. Phys. 11, 10565 (2009). 10.1039/B919565N
48. M. Paliy, R. Melnik, and B. A. Shapiro, Phys. Biol. 7, 036001 (2010). 10.1088/1478-3975/7/3/036001
49. F. Trovato and V. Tozzini, J. Phys. Chem. B 112, 13197 (2008). 10.1021/jp807085d
50. M. Sayar, B. Avarolu, and A. Kabakolu, Phys. Rev. E 81, 041916 (2010). 10.1103/PhysRevE.81.041916
51. P. D. Dans, A. Zeida, M. R. Machado, and S. Pantano, J. Chem. Theory Comput. 6, 1711 (2010). 10.1021/ct900653p
52. K. Voltz, J. Trylska, V. Tozzini, V. Kurkal-Siebert, J. Langowski, and J. Smith, J. Comput. Chem. 29, 1429 (2008). 10.1002/jcc.20902 (Pubitemid 351757766)
53. A. Morriss-Andrews, J. Rottler, and S. S. Plotkin, J. Chem. Phys. 132, 035105 (2010). 10.1063/1.3269994
54. A. A. Louis, J. Phys.: Condens. Matter 14, 9187 (2002). 10.1088/0953-8984/14/40/311 (Pubitemid 35275047)
55. M. E. Johnson, T. Head-Gordon, and A. A. Louis, J. Chem. Phys. 126, 144509 (2007). 10.1063/1.2715953 (Pubitemid 46610010)
56. K. Drukker, G. Wu, and G. C. Schatz, J. Chem. Phys. 114, 579 (2001). 10.1063/1.1329137 (Pubitemid 32088417)
57. M. Sales-Pardo, R. Guimera, A. A. Moreira, J. Widom, and L. Amaral, Phys. Rev. E 71, 051902 (2005). 10.1103/PhysRevE.71.051902 (Pubitemid 41480965)
58. M. Kenward and K. D. Dorfman, J. Chem. Phys. 130, 095101 (2009). 10.1063/1.3078795
59. F. Ding, S. Sharma, P. Chalasani, V. V. Demidov, N. E. Broude, and N. V. Dokholyan, RNA 14, 1164 (2008). 10.1261/rna.894608 (Pubitemid 351717496)
60. S. Pasquali and P. Derreumaux, J. Phys. Chem. B 114, 11957 (2010). 10.1021/jp102497y
61. C. Hyeon and D. Thirumalai, Proc. Natl. Acad. Sci. U.S.A. 102, 6789 (2005). 10.1073/pnas.0408314102 (Pubitemid 40675394)
62. C. Hyeon and D. Thirumulai, Biophys. J. 92, 731 (2007). 10.1529/biophysj.106.093062 (Pubitemid 46203206)
63. T. E. Ouldridge, I. G. Johnston, A. A. Louis, and J. P. K. Doye, J. Chem. Phys. 130, 065101 (2009). 10.1063/1.3055595
64. E. J. Sambriski, V. Ortiz, and J. J. de Pablo, J. Phys.: Condens. Matter 21 (2009). 10.1088/0953-8984/21/3/034105
65. E. J. Sambriski, D. C. Schwartz, and J. J. de Pablo, Biophys. J. 96, 1675 (2009). 10.1016/j.bpj.2008.09.061
66. S. Niewieczerza and M. Cieplak, J. Phys.: Condens. Matter 21, 474221 (2009). 10.1088/0953-8984/21/47/474221
67. T. E. Ouldridge, A. A. Louis, and J. P. K. Doye, Phys. Rev. Lett. 104, 178101 (2010). 10.1103/PhysRevLett.104.178101
68. S. Pitchiaya and Y. Krishnan, Chem. Soc. Rev. 35, 1111 (2006). 10.1039/b602886c (Pubitemid 44611724)
69. M. C. Murphy, I. Rasnik, W. Chang, T. M. Lohman, and T. Ha, Biophys. J. 86, 2530 (2004). 10.1016/S0006-3495(04)74308-8
70. J. Bois, S. Venkataraman, H. M.T. Choi, A. J. Spakowitz, Z. Wang, and N. A. Pierce, Nucleic Acids Res. 33, 4090 (2005). 10.1093/nar/gki721 (Pubitemid 41487269)
71. J. B. Mills, E. Vacano, and P. J. Hagerman, J. Mol. Biol. 285, 245 (1999). 10.1006/jmbi.1998.2287 (Pubitemid 29034041)
72. S. A. Harris, C. A. Laughton, and T. B. Liverpool, Nucleic Acids Res. 36, 21 (2008). 10.1093/nar/gkm891
73. T. Schlick, Molecular Modeling and Simulation (Springer-Verlag, New York, 2002).
74. S. Whitelam, E. H. Feng, M. F. Hagan, and P. L. Geissler, Soft Matter 5, 1521 (2009). 10.1039/b810031d
75. M. Swart, T. van der Wijst, C. F. Guerra, and F. M. Bickelhaupt, J. Mol. Model. 13, 1245 (2007). 10.1007/s00894-007-0239-y (Pubitemid 47629451)
76. J. Sponer, P. Jureka, I. Marchan, F. J. Luque, M. Orozco, and P. Hobza, Chem.-Eur. J. 12, 2854 (2006). 10.1002/chem.200501239
77. J. Holbrook, M. Capp, R. Saecker, and M. Record, Biochemistry 38, 8409 (1999). 10.1021/bi990043w (Pubitemid 29314214)
78. K. M. Guckan, B. A. Schweitzer, R. X.-F. Ren, C. J. Sheils, D. C. Tahmassebi, and E. T. Kool, J. Am. Chem. Soc. 122, 2213 (2000). 10.1021/ja9934854 (Pubitemid 30164632)
79. G. Torrie and J. P. Valleau, J. Comput. Phys. 23, 187 (1977). 10.1016/0021-9991(77)90121-8
80. S. Kumar, J. M. Rosenberg, D. Bouzida, R. H. Swendsen, and P. A. Kollman, J. Comput. Chem. 13, 1011 (1992). 10.1002/jcc.540130812
81. T. E. Ouldridge, A. A. Louis, and J. P.K. Doye, J. Phys.: Condens. Matter 22, 104102 (2010). 10.1088/0953-8984/22/10/104102
82. P. Chen and C. M. Li, Small 3, 1204 (2007). 10.1002/smll.200700049 (Pubitemid 47114376)
83. C. R. Calladine, H. R. Drew, B. F. Luisi, and A. A. Travers, Understanding DNA (Elsevier Academic, London, 2004).
84. G. Vesnaver and K. J. Breslauer, Proc. Natl. Acad. Sci. U.S.A. 88, 3569 (1991). 10.1073/pnas.88.9.3569
85. M. Leng and G. Felsenfeld, J. Mol. Biol. 15, 455 (1966). 10.1016/S0022-2836(66)80121-3
86. R. M. Epand and H. A. Scheraga, J. Am. Chem. Soc. 89, 3888 (1967). 10.1021/ja00991a036
87. D. Prschke, Biochemistry 15, 1495 (1976). 10.1021/bi00652a021
88. S. M. Freier, K. O. Hill, T. G. Dewey, L. A. Marky, and K. J. Breslauer, Biochemistry 20, 1419 (1981). 10.1021/bi00509a003
89. J. Zhou, S. Gregurick, S. Krueger, and F. Schwarz, Biophys. J. 90, 544 (2006). 10.1529/biophysj.105.071290
90. P. J. Mikulecky and A. L. Feig, Biopolymers 82, 38 (2006). 10.1002/bip.20457
91. J. Applequist and V. Damle, J. Am. Chem. Soc. 88, 3895 (1966). 10.1021/ja00969a001
92. I. Jelesarov, C. Crane-Robinson, and P. L. Privalov, J. Mol. Biol. 294, 981 (1999). 10.1006/jmbi.1999.3284 (Pubitemid 30000389)
93. -1 had a negligible effect.
94. D. Poland and H. A. Scheraga, Theory of Helix-Coil Transitions in Biopolymers: Statistical Mechanical Theory of Order-disorder Transitions in Biological Macromolecules (Academic, New York, 1970).
95. Our simulations are performed in the canonical ensemble, and hence should be described in terms of energy and entropy changes. We assume that, as dilute DNA strands contribute a very small partial pressure, discrepancies between constant volume and constant pressure results are small: we therefore use the term enthalpy to describe what are in fact energies in our model, for consistency with experimental literature.
96. Throughout this paper, lower case symbols represent enthalpy and entropy changes per pair of interacting bases, whereas capitals correspond to enthalpy and entropy changes per pair of interacting strands.
97. -4 M. Simulations of duplexes with more than 12 bp necessitated using a larger periodic cell, and hence a lower concentration. The fraction of bound duplexes was scaled to the higher concentration assuming the separate species are approximately ideal, as justified in Ref..
98. R. D. Blake and S. G. Delcourt, Nucleic Acids Res. 26, 3323 (1998). 10.1093/nar/26.14.3323 (Pubitemid 28321394)
99. M. D. Frank-Kamenetskii, Biopolymers 10, 2623 (1971). 10.1002/bip.360101223
100. D. Andreatta, S. Sen, J. L.P. Lustres, S. A. Kovalenko, N. P. Ernsting, C. J. Murphy, R. S. Coleman, and M. A. Berg, J. Am. Chem. Soc. 128, 6885 (2006). 10.1021/ja0582105 (Pubitemid 43830575)
101. S. Nonin, J.-L. Leroy, and M. Gueron, Biochemistry 34, 10652 (1995). 10.1021/bi00033a041
102. D. J. Patel and C. W. Hilbers, Biochemistry 14, 2651 (1975). 10.1021/bi00683a014
103. A. Tikhomirova, N. Taulier, and T. V. Chalikian, J. Am. Chem. Soc. 126, 16387 (2004). 10.1021/ja046387d (Pubitemid 40081936)
104. C. R. Cantor and P. R. Schimmel, Biophysical Chemistry Part III: The Behaviour of Biological Macromolecules (Freeman, San Francisco, 1980).
105. C. G. Baumann, S. B. Smith, V. A. Bloomfield, and C. Bustamante, Proc. Natl. Acad. Sci. U.S.A. 94, 6185 (1997). 10.1073/pnas.94.12.6185 (Pubitemid 27270659)
106. C. Rivetti, C. Walker, and C. Bustamante, J. Mol. Biol. 280, 41 (1998). 10.1006/jmbi.1998.1830 (Pubitemid 28312805)
107. M. Rubinstein and R. H. Colby, Polymer Physics (Oxford University Press, New York, 2003).
108. D. M. Crothers, J. Drak, J. D. Kahn, and S. D. Levene, Methods Enzymol. 212, 3 (1992). 10.1016/0076-6879(92)12003-9
109. M. Vologodskaia and A. Vologodskii, J. Mol. Biol. 317, 205 (2002). 10.1006/jmbi.2001.5366 (Pubitemid 34722188)
110. B. S. Fujimoto, G. P. Brewood, and J. M. Schurr, Biophys. J. 91, 4166 (2006). 10.1529/biophysj.106.087593 (Pubitemid 44887275)
111. Z. Bryant, M. D. Stone, J. Gore, S. B. Smith, N. R. Cozzarelli, and C. Bustamante, Nature (London) 424, 338 (2003). 10.1038/nature01810 (Pubitemid 36899378)
112. M. D. Wang, H. Yin, R. Landick, J. Gelles, and S. M. Block, Biophys. J. 72, 1335 (1997). 10.1016/S0006-3495(97)78780-0
113. J. R. Wenner, M. C. Williams, I. Rouzina, and V. A. Bloomfield, Biophys. J. 82, 3160 (2002). 10.1016/S0006-3495(02)75658-0
114. S. B. Smith, Y. Cui, and C. Bustamante, Science 271, 795 (1996). 10.1126/science.271.5250.795
115. T. Odijk, Macromolecules 28, 7016 (1995). 10.1021/ma00124a044
116. J. Gore, Z. Bryant, M. Nllman, M. U. Le, N. R. Cozzarelli, and C. Bustamante, Nature (London) 442, 836 (2006). 10.1038/nature04974 (Pubitemid 44258916)
117. T. Lionnet, S. Joubaud, R. Lavery, D. Bensimon, and V. Croquette, Phys. Rev. Lett. 96, 178102 (2006). 10.1103/PhysRevLett.96.178102
118. D. K. Hendrix, S. E. Brenner, and S. R. Holbrook, Q. Rev. Biophys. 38, 221 (2005). 10.1017/S0033583506004215 (Pubitemid 44268536)
119. S. Kuznetsov, Y. Shen, A. S. Benight, and A. Ansari, Biophys. J. 81, 2864 (2001). 10.1016/S0006-3495(01)75927-9
120. J. van Mameren, P. Gross, G. Farge, P. Hooijman, M. Modesti, M. Falkenberg, G. J. L. Wuite, and E. J.G. Peterman, Proc. Natl. Acad. Sci. U.S.A. 106, 18231 (2009). 10.1073/pnas.0904322106