Atomic force microscopy study of DNA flexibility on short length scales: Smooth bending versus kinking

Nucleic Acids Research

Volumn 42, Issue 22, 2014, Pages 14006-14012

  Mazur, Alexey K ^a   Maaloum, Mounir ^b  

^a France   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; DNA DETERMINATION; DNA FLEXIBILITY; DNA HELIX; DNA KINKING; DNA SMOOTH BENDING; ELASTICITY; GENETIC MODEL; GENETIC PARAMETERS; HYDROGEN BOND; IMAGE ANALYSIS; MATHEMATICAL COMPUTING; MONTE CARLO METHOD; PRIORITY JOURNAL; PROBABILITY; WORM LIKE CHAIN MODEL; ALGORITHM; CHEMISTRY; CONFORMATION; ULTRASTRUCTURE;

DNA;

ALGORITHMS; DNA; MICROSCOPY, ATOMIC FORCE; NUCLEIC ACID CONFORMATION;

EID: 84926360670     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1192     Document Type: Article

References (53)

1. Hagerman, P. J. (1988) Flexibility of DNA. Annu. Rev. Biophys. Biophys. Chem., 17, 265-286.
2. Travers, A. A. (1991) DNA bending and kinking - sequence dependence and function. Curr. Oppin. Struct. Biol., 1, 114-122.
3. Travers, A. A. (2004) The structural basis of DNA flexibility. Philos. Transact. A Math. Phys. Eng. Sci., 362, 1423-1438.
4. Peters, J. P. and Maher, L. J. (2010) DNA curvature and flexibility in vitro and in vivo. Q. Rev. Biophys., 43, 23-63.
5. Crick, F. H. C. and Klug, A. (1975) Kinky helix. Nature, 255, 530-533.
6. Namoradze, N. Z., Goryunov, A. N. and Birshtein, T. M. (1977) On conformations of the superhelix structure. Biophys. Chem., 7, 59-70.
7. Bresler, S. E. and Frenkel, Y. I. (1939) The character of thermal motion of long organic chains with reference to the elastic properties of rubber. Zh. Eksp. Teor. Fiz., 9, 1094-1106.
8. Landau, L. D. and Lifshitz, E. M. (1976) Statistical Physics, Part 1. Nauka, Moscow.
9. Cantor, C. R. and Schimmel, P. R. (1980) Biophysical Chemistry, Part III: The Behavior of Biological Macromolecules. W. H. Freeman, San Francisco, CA.
10. Nelson, P. C. (2012) Biochemistry. Spare the (elastic) rod. Science, 337, 1045-1046.
11. Cloutier, T. E. and Widom, J. (2004) Spontaneous sharp bending of double-stranded DNA. Mol. Cell, 14, 355-362.
12. 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.
13. Wiggins, P. A., Heijden, T. V. D., 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.
14. Yuan, C., Chen, H., Lou, X. W. and Archer, L. A. (2008) DNA bending stiffness on small length scales. Phys. Rev. Lett., 100, 018102.
15. Chen, H., Fu, H., Zhou, Z. and Yan, J. (2010) Non-harmonic DNA bending elasticity is revealed by statistics of DNA minicircle shapes. Int. J. Mod. Phys. B, 24, 5475-5485.
16. 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.
17. Altan-Bonnet, G., Libchaber, A. and Krichevsky, O. (2003) Bubble dynamics in double-stranded DNA. Phys. Rev. Lett., 90, 138101.
18. Yan, J. and Marko, J. F. (2004) Localized single-stranded bubble mechanism for cyclization of short double helix DNA. Phys. Rev. Lett., 93, 108108.
19. Zeng, Y., Montrichok, A. and Zocchi, G. (2004) Bubble nucleation and cooperativity in DNA melting. J. Mol. Biol., 339, 67-75.
20. Yan, J., Kawamura, R. and Marko, J. F. (2005) Statistics of loop formation along double helix DNAs. Phys. Rev. E, 71, 061905.
21. Wiggins, P. A., Phillips, R. and Nelson, P. C. (2005) Exact theory of kinkable elastic polymers. Phys. Rev. E, 71, 021909.
22. Ranjith, P., Sunil Kumar, P. B. and Menon, G. I. (2005) Distribution functions, loop formation probabilities, and force-extension relations in a model for short double-stranded DNA molecules. Phys. Rev. Lett., 94, 138102.
23. Yuan, C., Rhoades, E., Lou, X. W. and Archer, L. A. (2006) Spontaneous sharp bending of DNA: role of melting bubbles. Nucleic Acids Res., 34, 4554-4560.
24. Destainville, N., Manghi, M. and Palmeri, J. (2009) Microscopic mechanism for experimentally observed anomalous elasticity of DNA in two dimensions. Biophys. J., 96, 4464-4469.
25. 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.
26. Mazur, A. K. (2007) Wormlike chain theory and bending of short DNA. Phys. Rev. Lett., 98, 218102.
27. 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.
28. Linna, R. P. and Kaski, K. (2008) Analysis of DNA elasticity. Phys. Rev. Lett., 100, 168104.
29. Demurtas, D., Amzallag, A., Rawdon, E. J., Maddocks, J. H., Dubochet, J. and Stasiak, A. (2009) Bending modes of DNA directly addressed by cryo-electron microscopy of DNA minicircles. Nucleic Acids Res., 37, 2882-2893.
30. Mastroianni, A. J., Sivak, D. A., Geissler, P. L. and Alivisatos, A. P. (2009) Probing the conformational distributions of subpersistence length DNA. Biophys. J, 97, 1408-1417.
31. Forties, R. A., Bundschuh, R. and Poirier, M. G. (2009) The flexibility of locally melted DNA. Nucleic Acids Res., 37, 4580-4586.
32. Ortiz, V. and de Pablo, J. J. (2011) Molecular origins of DNA flexibility: sequence effects on conformational and mechanical properties. Phys. Rev. Lett., 106, 238107.
33. Schopflin, R., Brutzer, H., Muller, 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.
34. You, H., Iino, R., Watanabe, R. and Noji, H. (2012) Winding single-molecule double-stranded DNA on a nanometer-sized reel. Nucleic Acids Res., 40, e151.
35. Vologodskii, A., Du, Q. and Frank-Kamenetskii, M. D. (2013) Bending of short DNA helices. Artif. DNA: PNA XNA, 4, 1-3.
36. Vologodskii, A. and Frank-Kamenetskii, M. D. (2013) Strong bending of the DNA double helix. Nucleic Acids Res., 41, 6785-6792.
37. Han, W., Dlakic, M., Zhu, Y. J., Lindsay, S. M. and Harrington, R. E. (1997) Strained DNA is kinked by low concentrations of Zn2+. Proc. Natl Acad. Sci. U. S. A., 94, 10565-10570.
38. Pavlicek, J. W., Oussatcheva, E. A., Sinden, R. R., Potaman, V. N., Snakey, O. F. and Lyubchenko, Y. L. (2004) Supercoiling-induced DNA bending. Biochemistry, 43, 10664-10668.
39. Podesta, A., Indrieri, M., Brogioli, D., Manning, G. S., Milani, P., Guerra, R., Finzi, L. and Dunlap, D. (2005) Positively charged surfaces increase the flexibility of DNA. Biophys. J., 89, 2558-2563.
40. Moreno-Herrero, F., Seidel, R., Johnson, S. M., Fire, A. and Dekker, N. H. (2006) Structural analysis of hyperperiodic DNA from Caenorhabditis elegans. Nucleic Acids Res., 34, 3057-3066.
41. Zhang, J., McCauley, M. J. III, Maher, L. J., Williams, M. C. and Israeloff, N. E. (2009) Mechanism of DNA flexibility enhancement by HMGB proteins. Nucleic Acids Res., 37, 1107-1114.
42. 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, 3412-3416.
43. Hardin, A. H., Sarkar, S. K., Seol, Y., Liou, G. F., Osheroff, N. and Neuman, K. C. (2011) Direct measurement of DNA bending by type IIA topoisomerases: implications for non-equilibrium topology simplification. Nucleic Acids Res., 39, 5729-5743.
44. Buzio, R., Repetto, L., Giacopelli, F., Ravazzolo, R. and Valbusa, U. (2012) Label-free, atomic force microscopy-based mapping of DNA intrinsic curvature for the nanoscale comparative analysis of bent duplexes. Nucleic Acids Res., 40, e84.
45. Rivetti, C., Guthold, M. and Bustamante, C. (1996) Scanning force microscopy of DNA deposited onto mica: equilibration versus kinetic trapping studied by statistical polymer chain analysis. J. Mol. Biol., 264, 919-932.
46. Faas, F. G. A., Rieger, B., van Vliet, L. J. and Cherny, D. I. (2009) DNA deformations near charged surfaces: electron and atomic force microscopy views. Biophys. J., 97, 1148-1157.
47. Mazur, A. K. and Maaloum, M. (2014) DNA flexibility on short length scales probed by atomic force microscopy. Phys. Rev. Lett., 112, 068104.
48. Rivetti, C. and Codeluppi, S. (2001) Accurate length determination of DNA molecules visualized by atomic force microscopy: evidence for a partial B- to A-form transition on mica. Ultramicroscopy, 87, 55-66.
49. Calo, A., Stoliar, P., Bystrenova, E., Valle, F. and Biscarini, F. (2009) Measurement of DNA morphological parameters at highly entangled regime on surfaces. J. Phys. Chem. B, 113, 4987-4990.
50. Du, Q., Kotlyar, A. and Vologodskii, A. (2008) Kinking the double helix by bending deformation. Nucleic Acids Res., 36, 1120-1128.
51. Mazur, A. K. (2008) Statistics of time-limited ensembles of bent DNA conformations. J. Phys. Chem. B, 112, 4975-4982.
52. Han, W., Lindsay, S. M., Dlakic, M. and Harrington, R. E. (1997) Kinked DNA. Nature, 386, 563.
53. Mathew-Fenn, R. S., Das, R. and Harbury, P. A. B. (2008) Remeasuring the double helix. Science, 322, 446-449.