Probing the elastic limit of DNA bending

Nucleic Acids Research

Volumn 42, Issue 16, 2014, Pages 10786-10794

  Le, Tung T ^a   Kim, Harold D ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CURVED DNA; DOUBLE STRANDED DNA; DNA; MAGNESIUM;

ARTICLE; CONTROLLED STUDY; DNA DETERMINATION; DNA LOOP; DNA STABILITY; DNA STRUCTURE; ELASTICITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; LOOP SIZE; MECHANICAL STRESS; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; QUANTITATIVE ANALYSIS; STRUCTURE ANALYSIS; CHEMISTRY; CONFORMATION; DRUG EFFECTS;

DNA; ELASTICITY; FLUORESCENCE RESONANCE ENERGY TRANSFER; MAGNESIUM; NUCLEIC ACID CONFORMATION; STRESS, MECHANICAL;

EID: 84917687684     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku735     Document Type: Article

References (70)

1. Olson, W. K. and Zhurkin, V. B. Olson, W. K. and Zhurkin, V. B. (2000) Modeling DNA deformations. Curr. Opin. Struct. Biol., 10, 286-297.
2. Strick, T., Allemand, J., Croquette, V., and Bensimon, D. Strick, T., Allemand, J., Croquette, V., and Bensimon, D. (2000) Twisting and stretching single DNA molecules. Prog. Biophys. Mol. Biol., 74, 115-140.
3. Nikolova, E. N., Kim, E., Wise, A. A., O'Brien, P. J., Andricioaei, I., and Al-Hashimi, H. M. Nikolova, E. N., Kim, E., Wise, A. A., O'Brien, P. J., Andricioaei, I., and Al-Hashimi, H. M. (2011) Transient Hoogsteen base pairs in canonical duplex DNA. Nature, 470, 498-502.
4. Maehigashi, T., Hsiao, C., Kruger Woods, K., Moulaei, T., Hud, N. V., and Dean Williams, L. Maehigashi, T., Hsiao, C., Kruger Woods, K., Moulaei, T., Hud, N. V., and Dean Williams, L. (2012) B-DNA structure is intrinsically polymorphic: even at the level of base pair positions. Nucleic Acids Res., 40, 3714-3722.
5. Shimada, J. and Yamakawa, H. Shimada, J. and Yamakawa, H. (1984) Ring-closure probabilities for twisted wormlike chains. Application to DNA. Macromolecules, 17, 689-698.
6. Samuel Frederick, E. Samuel Frederick, E. (1986) In: The Theory of Polymer Dynamics, Clarendon, Oxford.
7. Elias, J. G. and Eden, D. Elias, J. G. and Eden, D. (1981) Transient electric birefringence study of the persistence length and electrical polarizability of restriction fragments of DNA. Macromolecules, 14, 410-419.
8. Bednar, J., Furrer, P., Katritch, V., Stasiak, A., Dubochet, J., and Stasiak, A. Bednar, J., Furrer, P., Katritch, V., Stasiak, A., Dubochet, J., and Stasiak, A. (1995) Determination of DNA persistence length by cryo-electron microscopy. Separation of the static and dynamic contributions to the apparent persistence length of DNA. J. Mol. Biol., 254, 579-594.
9. Smith, S. B., Cui, Y., and Bustamante, C. Smith, S. B., Cui, Y., and Bustamante, C. (1996) Overstretching B-DNA: the elastic response of individual double-stranded and single-stranded DNA molecules. Science, 271, 795-799.
10. Bouchiat, C., Wang, M. D., Allemand, J. -F., Strick, T., Block, S. M., and Croquette, V. Bouchiat, C., Wang, M. D., Allemand, J. -F., Strick, T., Block, S. M., and Croquette, V. (1999) Estimating the persistence length of a worm-like chain molecule from force-extension measurements. Biophys. J., 76, 409-413.
11. Shore, D., Langowski, J., and Baldwin, R. L. Shore, D., Langowski, J., and Baldwin, R. L. (1981) DNA flexibility studied by covalent closure of short fragments into circles. Proc. Natl Acad. Sci., 78, 4833-4837.
12. Taylor, W. H. and Hagerman, P. J. Taylor, W. H. and Hagerman, P. J. (1990) Application of the method of phage T4 DNA ligase-catalyzed ring-closure to the study of DNA structure. II. NaCl-dependence of DNA flexibility and helical repeat. J. Mol. Biol., 212, 363-376.
13. Geggier, S. and Vologodskii, A. Geggier, S. and Vologodskii, A. (2010) Sequence dependence of DNA bending rigidity. Proc. Natl Acad. Sci., 107, 15421-15426.
14. Geggier, S., Kotlyar, A., and Vologodskii, A. Geggier, S., Kotlyar, A., and Vologodskii, A. (2011) Temperature dependence of DNA persistence length. Nucleic Acids Res., 39, 1419-1426.
15. Porschke, D. Porschke, D. (1991) Persistence length and bending dynamics of DNA from electrooptical measurements at high salt concentrations. Biophys. Chem., 40, 169-179.
16. Baumann, C. G., Smith, S. B., Bloomfield, V. A., and Bustamante, C. Baumann, C. G., Smith, S. B., Bloomfield, V. A., and Bustamante, C. (1997) Ionic effects on the elasticity of single DNA molecules. Proc. Natl Acad. Sci., 94, 6185-6190.
17. Wenner, J. R., Williams, M. C., Rouzina, I., and Bloomfield, V. A. Wenner, J. R., Williams, M. C., Rouzina, I., and Bloomfield, V. A. (2002) Salt dependence of the elasticity and overstretching transition of single DNA molecules. Biophys. J., 82, 3160-3169.
18. Garcia, H. G., Grayson, P., Han, L., Inamdar, M., Kondev, J., Nelson, P. C., Phillips, R., Widom, J., and Wiggins, P. A. Garcia, H. G., Grayson, P., Han, L., Inamdar, M., Kondev, J., Nelson, P. C., Phillips, R., Widom, J., and Wiggins, P. A. (2007) Biological consequences of tightly bent DNA: the other life of a macromolecular celebrity. Biopolymers, 85, 115-130.
19. Cloutier, T. E. and Widom, J. Cloutier, T. E. and Widom, J. (2004) Spontaneous sharp bending of double-stranded DNA. Mol. Cell, 14, 355-362.
20. Cloutier, T. E. and Widom, J. Cloutier, T. E. and Widom, J. (2005) DNA twisting flexibility and the formation of sharply looped protein-DNA complexes. Proc. Natl Acad. Sci. U. S. A., 102, 3645-3650.
21. Wiggins, P. A., van der Heijden, T., Moreno-Herrero, F., Spakowitz, A., Phillips, R., Widom, J., Dekker, C., and Nelson, P. C. Wiggins, P. A., van der Heijden, T., Moreno-Herrero, F., Spakowitz, A., Phillips, R., Widom, J., Dekker, C., and Nelson, P. C. (2006) High flexibility of DNA on short length scales probed by atomic force microscopy. Nat. Nanotechnol., 1, 137-141.
22. Du, Q., Smith, C., Shiffeldrim, N., Vologodskaia, M., and Vologodskii, A. Du, Q., Smith, C., Shiffeldrim, N., Vologodskaia, M., and Vologodskii, A. (2005) Cyclization of short DNA fragments and bending fluctuations of the double helix. Proc. Natl Acad. Sci. U. S. A., 102, 5397-5402.
23. Mazur, A. K. and Maaloum, M. Mazur, A. K. and Maaloum, M. (2014) DNA flexibility on short length scales probed by atomic force microscopy. Phys. Rev. Lett., 112, 068104.
24. Vafabakhsh, R. and Ha, T. Vafabakhsh, R. and Ha, T. (2012) Extreme bendability of DNA less than 100 base pairs long revealed by single-molecule cyclization. Science, 337, 1097-1101.
25. Yuan, C., Lou, X. W., Rhoades, E., Chen, H., and Archer, L. A. Yuan, C., Lou, X. W., Rhoades, E., Chen, H., and Archer, L. A. (2007) T4 DNA ligase is more than an effective trap of cyclized dsDNA. Nucleic Acids Res., 35, 5294-5302.
26. Manzo, C., Zurla, C., Dunlap, D. D., and Finzi, L. Manzo, C., Zurla, C., Dunlap, D. D., and Finzi, L. (2012) The effect of nonspecific binding of lambda repressor on DNA looping dynamics. Biophys. J., 103, 1753-1761.
27. Han, L., Garcia, H. G., Blumberg, S., Towles, K. B., Beausang, J. F., Nelson, P. C., and Phillips, R. Han, L., Garcia, H. G., Blumberg, S., Towles, K. B., Beausang, J. F., Nelson, P. C., and Phillips, R. (2009) Concentration and length dependence of DNA looping in transcriptional regulation. PLoS One, 4, e5621.
28. Vologodskii, A. and Frank-Kamenetskii, M. D. Vologodskii, A. and Frank-Kamenetskii, M. D. (2013) Strong bending of the DNA double helix. Nucleic Acids Res., 41, 6785-6792.
29. Brukner, I., Susic, S., Dlakic, M., Savic, A., and Pongor, S. Brukner, I., Susic, S., Dlakic, M., Savic, A., and Pongor, S. (1994) Physiological concentration of magnesium ions induces a strong macroscopic curvature in GGGCCC-containing DNA. J. Mol. Biol., 236, 26-32.
30. Rouzina, I. and Bloomfield, V. A. Rouzina, I. and Bloomfield, V. A. (1998) DNA bending by small, mobile multivalent cations. Biophys. J., 74, 3152-3164.
31. Williams, L. D. and Maher, L. J. IIIWilliams, L. D. and Maher, L. J. III (2000) Electrostatic mechanisms of DNA deformation. Annu. Rev. Biophys. Biomol. Struct., 29, 497-521.
32. Stellwagen, N. C. and Lu, Y. Stellwagen, N. C. and Lu, Y. (2010) Effect of magnesium ions and temperature on the sequence-dependent curvature of DNA restriction fragments. J. Phys. Condens. Matter, 22, 494110.
33. Peters, J. P. and Maher, L. J. Peters, J. P. and Maher, L. J. (2010) DNA curvature and flexibility in vitro and in vivo. Q. Rev. Biophys., 43, 23-63.
34. Vologodskii, A., Du, Q., and Frank-Kamenetskii, M. D. Vologodskii, A., Du, Q., and Frank-Kamenetskii, M. D. (2013) Bending of short DNA helices. Artif. DNA PNA XNA, 4, 1-3.
35. Le, T. T. and Kim, H. D. Le, T. T. and Kim, H. D. (2013) Measuring shape-dependent looping probability of DNA. Biophys. J., 104, 2068-2076.
36. Le, T. T. and Kim, H. D. Le, T. T. and Kim, H. D. (2014) Studying DNA looping by single-molecule FRET. J. Vis. Exp., 88, e51667.
37. Wiggins, P. A. and Nelson, P. C. Wiggins, P. A. and Nelson, P. C. (2006) Generalized theory of semiflexible polymers. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 73, 031906.
38. Du, Q., Vologodskaia, M., Kuhn, H., Frank-Kamenetskii, M., and Vologodskii, A. Du, Q., Vologodskaia, M., Kuhn, H., Frank-Kamenetskii, M., and Vologodskii, A. (2005) Gapped DNA and cyclization of short DNA fragments. Biophys. J., 88, 4137-4145.
39. Shore, D. and Baldwin, R. L. Shore, D. and Baldwin, R. L. (1983) Energetics of DNA twisting: I. Relation between twist and cyclization probability. J. Mol. Biol., 170, 957-981.
40. Kastner, J. and Thiel, W. Kastner, J. and Thiel, W. (2005) Bridging the gap between thermodynamic integration and umbrella sampling provides a novel analysis method: 'Umbrella integration'. J. Chem. Phys., 123, 144104.
41. Hwang, W. Hwang, W. (2007) Calculation of conformation-dependent biomolecular forces. J. Chem. Phys., 127, 175104.
42. Kumar, S., Rosenberg, J. M., Bouzida, D., Swendsen, R. H., and Kollman, P. A. Kumar, S., Rosenberg, J. M., Bouzida, D., Swendsen, R. H., and Kollman, P. A. (1992) THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J. Comput. Chem., 13, 1011-1021.
43. Becker, N. B., Rosa, A., and Everaers, R. Becker, N. B., Rosa, A., and Everaers, R. (2010) The radial distribution function of worm-like chains. Eur. Phys. J. E Soft Matter, 32, 53-69.
44. Zheng, X. and Vologodskii, A. Zheng, X. and Vologodskii, A. (2009) Theoretical analysis of disruptions in DNA minicircles. Biophys. J., 96, 1341-1349.
45. Bell, G. I. Bell, G. I. (1978) Models for the specific adhesion of cells to cells. Science, 200, 618-627.
46. Bustamante, C., Chemla, Y. R., Forde, N. R., and Izhaky, D. Bustamante, C., Chemla, Y. R., Forde, N. R., and Izhaky, D. (2004) Mechanical processes in biochemistry. Annu. Rev. Biochem., 73, 705-748.
47. Douarche, N. and Cocco, S. Douarche, N. and Cocco, S. (2005) Protein-mediated DNA loops: effects of protein bridge size and kinks. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 72, 061902.
48. Allemand, J. -F., Cocco, S., Douarche, N., and Lia, G. Allemand, J. -F., Cocco, S., Douarche, N., and Lia, G. (2006) Loops in DNA: an overview of experimental and theoretical approaches. Eur. Phys. J. E Soft Matter, 19, 293-302.
49. Strunz, T., Oroszlan, K., Schäfer, R., and Güntherodt, H. -J. Strunz, T., Oroszlan, K., Schäfer, R., and Güntherodt, H. -J. (1999) Dynamic force spectroscopy of single DNA molecules. Proc. Natl Acad. Sci., 96, 11277-11282.
50. Hinczewski, M., Gebhardt, J. C. M., Rief, M., and Thirumalai, D. Hinczewski, M., Gebhardt, J. C. M., Rief, M., and Thirumalai, D. (2013) From mechanical folding trajectories to intrinsic energy landscapes of biopolymers. Proc. Natl Acad. Sci., 110, 4500-4505.
51. Evans, E., Leung, A., Heinrich, V., and Zhu, C. Evans, E., Leung, A., Heinrich, V., and Zhu, C. (2004) Mechanical switching and coupling between two dissociation pathways in a P-selectin adhesion bond. Proc. Natl Acad. Sci. U. S. A., 101, 11281-11286.
52. Comstock, M. J., Ha, T., and Chemla, Y. R. Comstock, M. J., Ha, T., and Chemla, Y. R. (2011) Ultrahigh-resolution optical trap with single-fluorophore sensitivity. Nat. Methods, 8, 335-340.
53. Agrawal, N. J., Radhakrishnan, R., and Purohit, P. K. Agrawal, N. J., Radhakrishnan, R., and Purohit, P. K. (2008) Geometry of mediating protein affects the probability of loop formation in DNA. Biophys. J., 94, 3150-3158.
54. Crick, F. H. C. and Klug, A. Crick, F. H. C. and Klug, A. (1975) Kinky helix. Nature, 255, 530-533.
55. Zeida, A., Machado, M. R., Dans, P. D., and Pantano, S. Zeida, A., Machado, M. R., Dans, P. D., and Pantano, S. (2012) Breathing, bubbling, and bending: DNA flexibility from multimicrosecond simulations. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 86, 021903.
56. Frank-Kamenetskii, M. D. and Prakash, S. Frank-Kamenetskii, M. D. and Prakash, S. (2014) Fluctuations in the DNA double helix: a critical review. Phys. Life Rev., 11, 153-170.
57. Lankaš, F., Lavery, R., and Maddocks, J. H. Lankaš, F., Lavery, R., and Maddocks, J. H. (2006) Kinking occurs during molecular dynamics simulations of small DNA minicircles. Structure, 14, 1527-1534.
58. Lee, O. and Sung, W. Lee, O. and Sung, W. (2012) Enhanced bubble formation in looped short double-stranded DNA. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 85, 021902.
59. Fields, A. P., Meyer, E. A., and Cohen, A. E. Fields, A. P., Meyer, E. A., and Cohen, A. E. (2013) Euler buckling and nonlinear kinking of double-stranded DNA. Nucleic Acids Res., 41, 9881-9890.
60. Wiggins, P. A., Phillips, R., and Nelson, P. C. Wiggins, P. A., Phillips, R., and Nelson, P. C. (2005) Exact theory of kinkable elastic polymers. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 71, 021909.
61. Yan, J. and Marko, J. F. Yan, J. and Marko, J. F. (2004) Localized single-stranded bubble mechanism for cyclization of short double helix DNA. Phys. Rev. Lett., 93, 108108.
62. Ranjith, P., Kumar, P., and Menon, G. Ranjith, P., Kumar, P., and Menon, G. (2005) Distribution functions, loop formation probabilities, and force-extension relations in a model for short double-stranded DNA molecules. Phys. Rev. Lett., 94, 138102.
63. Sivak, D. A. and Geissler, P. L. Sivak, D. A. and Geissler, P. L. (2012) Consequences of local inter-strand dehybridization for large-amplitude bending fluctuations of double-stranded DNA. J. Chem. Phys., 136, 045102.
64. Mitchell, J. S., Laughton, C. A., and Harris, S. A. Mitchell, J. S., Laughton, C. A., and Harris, S. A. (2011) Atomistic simulations reveal bubbles, kinks and wrinkles in supercoiled DNA. Nucleic Acids Res., 39, 3928-3938.
65. Du, Q., Kotlyar, A., and Vologodskii, A. Du, Q., Kotlyar, A., and Vologodskii, A. (2008) Kinking the double helix by bending deformation. Nucleic Acids Res., 36, 1120-1128.
66. Schöpflin, R., Brutzer, H., Müller, O., Seidel, R., and Wedemann, G. Schöpflin, R., Brutzer, H., Müller, O., Seidel, R., and Wedemann, G. (2012) Probing the elasticity of DNA on short length scales by modeling supercoiling under Tension. Biophys. J., 103, 323-330.
67. Shi, X., Herschlag, D., and Harbury, P. A. B. Shi, X., Herschlag, D., and Harbury, P. A. B. (2013) Structural ensemble and microscopic elasticity of freely diffusing DNA by direct measurement of fluctuations. Proc. Natl Acad. Sci., 110, E1444-E1451.
68. Mantelli, S., Muller, P., Harlepp, S., and Maaloum, M. Mantelli, S., Muller, P., Harlepp, S., and Maaloum, M. (2011) Conformational analysis and estimation of the persistence length of DNA using atomic force microscopy in solution. Soft Matter, 7, 3412.
69. Shroff, H., Sivak, D., Siegel, J. J., McEvoy, A. L., Siu, M., Spakowitz, A., Geissler, P. L., and Liphardt, J. Shroff, H., Sivak, D., Siegel, J. J., McEvoy, A. L., Siu, M., Spakowitz, A., Geissler, P. L., and Liphardt, J. (2008) Optical measurement of mechanical forces inside short DNA loops. Biophys. J., 94, 2179-2186.
70. Wang, J., Qu, H., and Zocchi, G. Wang, J., Qu, H., and Zocchi, G. (2013) Critical bending torque of DNA is a materials parameter independent of local base sequence. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 88, 032712.