Browse > Article
http://dx.doi.org/10.14348/molcells.2021.0182

Single-Molecule Methods for Investigating the Double-Stranded DNA Bendability  

Yeou, Sanghun (Department of Physics, Pohang University of Science and Technology)
Lee, Nam Ki (Department of Chemistry, Seoul National University)
Publication Information
Molecules and Cells / v.45, no.1, 2022 , pp. 33-40 More about this Journal
Abstract
The various DNA-protein interactions associated with the expression of genetic information involve double-stranded DNA (dsDNA) bending. Due to the importance of the formation of the dsDNA bending structure, dsDNA bending properties have long been investigated in the biophysics field. Conventionally, DNA bendability is characterized by innate averaging data from bulk experiments. The advent of single-molecule methods, such as atomic force microscopy, optical and magnetic tweezers, tethered particle motion, and single-molecule fluorescence resonance energy transfer measurement, has provided valuable tools to investigate not only the static structures but also the dynamic properties of bent dsDNA. Here, we reviewed the single-molecule methods that have been used for investigating dsDNA bendability and new findings related to dsDNA bending. Single-molecule approaches are promising tools for revealing the unknown properties of dsDNA related to its bending, particularly in cells.
Keywords
DNA bending; fluorescence resonance energy transfer; persistence length; polymer mechanics; single-molecule techniques;
Citations & Related Records
Times Cited By KSCI : 3  (Citation Analysis)
연도 인용수 순위
1 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.   DOI
2 Yakovchuk, P., Protozanova, E., and Frank-Kamenetskii, M.D. (2006). Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res. 34, 564-574.   DOI
3 Yoo, J. (2021). On the stability of protein-DNA complexes in molecular dynamics simulations using the CUFIX corrections. J. Korean Phys. Soc. 78, 461-466.   DOI
4 Yoo, J., Kim, H., Aksimentiev, A., and Ha, T. (2016). Direct evidence for sequence-dependent attraction between double-stranded DNA controlled by methylation. Nat. Commun. 7, 11045.   DOI
5 Qu, H., Wang, Y., Tseng, C.Y., and Zocchi, G. (2011). Critical torque for kink formation in double-stranded DNA. Phys. Rev. X 1, 021008.
6 Driessen, R.P.C., Sitters, G., Laurens, N., Moolenaar, G.F., Wuite, G.J.L., Goosen, N., and Dame, R.T. (2014). Effect of temperature on the intrinsic flexibility of DNA and its interaction with architectural proteins. Biochemistry 53, 6430-6438.   DOI
7 Prinsen, P. and Schiessel, H. (2010). Nucleosome stability and accessibility of its DNA to proteins. Biochimie 92, 1722-1728.   DOI
8 Saran, R., Wang, Y., and Li, I.T.S. (2020). Mechanical flexibility of DNA: a quintessential tool for DNA nanotechnology. Sensors (Basel) 20, 7019.   DOI
9 Kang, Y., Cho, C., Lee, K.S., Song, J.J., and Lee, J.Y. (2021). Single-molecule imaging reveals the mechanism underlying histone loading of Schizosaccharomyces pombe AAA+ ATPase Abo1. Mol. Cells 44, 79-87.   DOI
10 Bhairosing-Kok, D., Groothuizen, F.S., Fish, A., Dharadhar, S., Winterwerp, H.H.K., and Sixma, T.K. (2019). Sharp kinking of a coiled-coil in MutS allows DNA binding and release. Nucleic Acids Res. 47, 8888-8898.   DOI
11 Ashkin, A. (1997). Optical trapping and manipulation of neutral particles usinglasers. Proc. Natl. Acad. Sci. U. S. A. 94, 4853-4860.   DOI
12 Basu, A., Bobrovnikov, D.G., and Ha, T. (2021a). DNA mechanics and its biological impact. J. Mol. Biol. 433, 166861.   DOI
13 Ashkin, A., Dziedzic, J.M., Bjorkholm, J.E., and Chu, S. (1986). Observation of a single-beam gradient force optical trap for dielectric particles. Opt. Lett. 11, 288-290.   DOI
14 Ben-Shaul, A. (2013). Entropy, energy, and bending of DNA in viral capsids. Biophys. J. 104, L15-L17.   DOI
15 Binnig, G., Quate, C.F., and Gerber, C. (1986). Atomic force microscope. Phys. Rev. Lett. 56, 930-933.   DOI
16 Baumann, C.G., Bloomfield, V.A., Smith, S.B., Bustamante, C., Wang, M.D., and Block, S.M. (2000). Stretching of single collapsed DNA molecules. Biophys. J. 78, 1965-1978.   DOI
17 Brahmachari, S. and Marko, J.F. (2018). DNA mechanics and topology. In Biomechanics in Oncology, C. Dong, N. Zahir, and K. Konstantopoulos, eds. (Cham: Springer International Publishing), pp. 11-39.
18 Brunet, A., Salome, L., Rousseau, P., Destainville, N., Manghi, M., and Tardin, C. (2018). How does temperature impact the conformation of single DNA molecules below melting temperature? Nucleic Acids Res. 46, 2074-2081.   DOI
19 Basu, A., Bobrovnikov, D.G., Qureshi, Z., Kayikcioglu, T., Ngo, T.T.M., Ranjan, A., Eustermann, S., Cieza, B., Morgan, M.T., Hejna, M., et al. (2021b). Measuring DNA mechanics on the genome scale. Nature 589, 462-467.   DOI
20 Brinkers, S., Dietrich, H.R.C., de Groote, F.H., Young, I.T., and Rieger, B. (2009). The persistence length of double stranded DNA determined using dark field tethered particle motion. J. Chem. Phys. 130, 215105.   DOI
21 Brunet, A., Chevalier, S., Destainville, N., Manghi, M., Rousseau, P., Salhi, M., Salome, L., and Tardin, C. (2015a). Probing a label-free local bend in DNA by single molecule tethered particle motion. Nucleic Acids Res. 43, e72.   DOI
22 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.   DOI
23 Cloutier, T.E. and Widom, J. (2004). Spontaneous sharp bending of double-stranded DNA. Mol. Cell 14, 355-362.   DOI
24 Fan, H.F., Ma, C.H., and Jayaram, M. (2018). Single-molecule tethered particle motion: stepwise analyses of site-specific DNA recombination. Micromachines (Basel) 9, 216.   DOI
25 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.   DOI
26 Forster, T. (1946). [Energiewanderung und Fluoreszenz]. Naturwissenschaften 33, 166-175. German.   DOI
27 Forties, R.A., Bundschuh, R., and Poirier, M.G. (2009). The flexibility of locally melted DNA. Nucleic Acids Res. 37, 4580-4586.   DOI
28 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.   DOI
29 Guilbaud, S., Salome, L., Destainville, N., Manghi, M., and Tardin, C. (2019). Dependence of DNA persistence length on ionic strength and ion type. Phys. Rev. Lett. 122, 028102.   DOI
30 Hagerman, P.J. (1988). Flexibility of DNA. Annu. Rev. Biophys. Biophys. Chem. 17, 265-286.   DOI
31 Cai, X., Arias, D.S., Velazquez, L.R., Vexler, S., Bevier, A.L., and Fygenson, D.K. (2020). DNA nunchucks: nanoinstrumentation for single-molecule measurement of stiffness and bending. Nano Lett. 20, 1388-1395.   DOI
32 Kim, C., Lee, O.C., Kim, J.Y., Sung, W., and Lee, N.K. (2015). Dynamic release of bending stress in short dsDNA by formation of a kink and forks. Angew. Chem. Int. Ed. Engl. 54, 8943-8947.   DOI
33 Hildebrandt, L.L., Preus, S., and Birkedal, V. (2015). Quantitative single molecule FRET efficiencies using TIRF microscopy. Faraday Discuss. 184, 131-142.   DOI
34 Jeong, J. and Kim, H.D. (2020). Determinants of cyclization-decyclization kinetics of short DNA with sticky ends. Nucleic Acids Res. 48, 5147-5156.   DOI
35 Lerner, E., Barth, A., Hendrix, J., Ambrose, B., Birkedal, V., Blanchard, S.C., Borner, R., Sung Chung, H., Cordes, T., Craggs, T.D., et al. (2021). FRET-based dynamic structural biology: challenges, perspectives and an appeal for open-science practices. Elife 10, e60416.   DOI
36 Kang, J., Jung, J., and Kim, S.K. (2014). Flexibility of single-stranded DNA measured by single-molecule FRET. Biophys. Chem. 195, 49-52.   DOI
37 Kratky, O. and Porod, G. (1949). [Rontgenuntersuchung geloster Fadenmolekule]. Recl. Trav. Chim. Pays Bas 68, 1106-1122. German.   DOI
38 Lee, D.H. and Schleif, R.F. (1989). In vivo DNA loops in araCBAD: size limits and helical repeat. Proc. Natl. Acad. Sci. U. S. A. 86, 476-480.   DOI
39 Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F., and Richmond, T.J. (1997). Crystal structure of the nucleosome core particle at 2.8A resolution. Nature 389, 251-260.   DOI
40 Murphy, M.C., Rasnik, I., Cheng, W., Lohman, T.M., and Ha, T. (2004). Probing single-stranded DNA conformational flexibility using fluorescence spectroscopy. Biophys. J. 86, 2530-2537.   DOI
41 Kim, S.H., Kim, H., Jeong, H., and Yoon, T.Y. (2021b). Encoding multiple virtual signals in DNA barcodes with single-molecule FRET. Nano Lett. 21, 1694-1701.   DOI
42 Geggier, S., Kotlyar, A., and Vologodskii, A. (2011). Temperature dependence of DNA persistence length. Nucleic Acids Res. 39, 1419-1426.   DOI
43 Geggier, S. and Vologodskii, A. (2010). Sequence dependence of DNA bending rigidity. Proc. Natl. Acad. Sci. U. S. A. 107, 15421-15426.   DOI
44 Kapanidis, A.N., Lee, N.K., Laurence, T.A., Doose, S., Margeat, E., and Weiss, S. (2004). Fluorescence-aided molecule sorting: analysis of structure and interactions by alternating-laser excitation of single molecules. Proc. Natl. Acad. Sci. U. S. A. 101, 8936-8941.   DOI
45 Ha, T., Enderle, T., Ogletree, D.F., Chemla, D.S., Selvin, P.R., and Weiss, S. (1996). Probing the interaction between two single molecules: fluorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. U. S. A. 93, 6264-6268.   DOI
46 Hellenkamp, B., Schmid, S., Doroshenko, O., Opanasyuk, O., Kuhnemuth, R., Rezaei Adariani, S., Ambrose, B., Aznauryan, M., Barth, A., Birkedal, V., et al. (2018). Precision and accuracy of single-molecule FRET measurements-a multi-laboratory benchmark study. Nat. Methods 15, 669-676.   DOI
47 Jeong, J. and Kim, H.D. (2019). Base-pair mismatch can destabilize small DNA loops through cooperative kinking. Phys. Rev. Lett. 122, 218101.   DOI
48 Kim, S., Song, H.S., Yu, J., and Kim, Y.M. (2021a). MiT family transcriptional factors in immune cell functions. Mol. Cells 44, 342-355.   DOI
49 Le, T.T. and Kim, H.D. (2014). Probing the elastic limit of DNA bending. Nucleic Acids Res. 42, 10786-10794.   DOI
50 Lee, O.C., Kim, C., Kim, J.Y., Lee, N.K., and Sung, W. (2016). Two conformational states in D-shaped DNA: effects of local denaturation. Sci. Rep. 6, 28239.   DOI
51 Marko, J.F. and Siggia, E.D. (1995). Stretching DNA. Macromolecules 28, 8759-8770.   DOI
52 Purohit, P.K., Kondev, J., and Phillips, R. (2003). Mechanics of DNA packaging in viruses. Proc. Natl. Acad. Sci. U. S. A. 100, 3173-3178.   DOI
53 Ngo, T.T.M., Yoo, J., Dai, Q., Zhang, Q., He, C., Aksimentiev, A., and Ha, T. (2016). Effects of cytosine modifications on DNA flexibility and nucleosome mechanical stability. Nat. Commun. 7, 10813.   DOI
54 Pavlicek, J.W., Oussatcheva, E.A., Sinden, R.R., Potaman, V.N., Sankey, O.F., and Lyubchenko, Y.L. (2004). Supercoiling-induced DNA bending. Biochemistry 43, 10664-10668.   DOI
55 Protozanova, E., Yakovchuk, P., and Frank-Kamenetskii, M.D. (2004). Stacked-unstacked equilibrium at the nick site of DNA. J. Mol. Biol. 342, 775-785.   DOI
56 Ray, P.C., Fan, Z., Crouch, R.A., Sinha, S.S., and Pramanik, A. (2014). Nanoscopic optical rulers beyond the FRET distance limit: fundamentals and applications. Chem. Soc. Rev. 43, 6370-6404.   DOI
57 Roth, E., Glick Azaria, A., Girshevitz, O., Bitler, A., and Garini, Y. (2018). Measuring the conformation and persistence length of single-stranded DNA using a DNA origami structure. Nano Lett. 18, 6703-6709.   DOI
58 Schafer, D.A., Gelles, J., Sheetz, M.P., and Landick, R. (1991). Transcription by single molecules of RNA polymerase observed by light microscopy. Nature 352, 444-448.   DOI
59 Shore, D., Langowski, J., and Baldwin, R.L. (1981). DNA flexibility studied by covalent closure of short fragments into circles. Proc. Natl. Acad. Sci. U. S. A. 78, 4833-4837.   DOI
60 Brunet, A., Tardin, C., Salome, L., Rousseau, P., Destainville, N., and Manghi, M. (2015b). Dependence of DNA persistence length on ionic strength of solutions with monovalent and divalent salts: a joint theory-experiment study. Macromolecules 48, 3641-3652.   DOI
61 Peters, J.P. and Maher, L.J. (2018). Approaches for determining DNA persistence length using atomic force microscopy. In Bacterial Chromatin: Methods and Protocols, R.T. Dame, ed. (New York: Springer New York), pp. 211-256.
62 Slutsky, M. (2005). Diffusion in a half-space: from Lord Kelvin to path integrals. Am. J. Phys. 73, 308-314.   DOI
63 Shroff, H., Reinhard, B.M., Siu, M., Agarwal, H., Spakowitz, A., and Liphardt, J. (2005). Biocompatible force sensor with optical readout and dimensions of 6 nm3. Nano Lett. 5, 1509-1514.   DOI
64 Nathan, D. and Crothers, D.M. (2002). Bending and flexibility of methylated and unmethylated EcoRI DNA. J. Mol. Biol. 316, 7-17.   DOI
65 Pongor, C.I., Bianco, P., Ferenczy, G., Kellermayer, R., and Kellermayer, M. (2017). Optical trapping nanometry of hypermethylated CpG-island DNA. Biophys. J. 112, 512-522.   DOI
66 Privalov, P.L., Dragan, A.I., and Crane-Robinson, C. (2009). The cost of DNA bending. Trends Biochem. Sci. 34, 464-470.   DOI
67 Shon, M.J., Rah, S.H., and Yoon, T.Y. (2019). Submicrometer elasticity of double-stranded DNA revealed by precision force-extension measurements with magnetic tweezers. Sci. Adv. 5, eaav1697.   DOI
68 Pyne, A.L.B., Noy, A., Main, K.H.S., Velasco-Berrelleza, V., Piperakis, M.M., Mitchenall, L.A., Cugliandolo, F.M., Beton, J.G., Stevenson, C.E.M., Hoogenboom, B.W., et al. (2021). Base-pair resolution analysis of the effect of supercoiling on DNA flexibility and major groove recognition by triplex-forming oligonucleotides. Nat. Commun. 12, 1053.   DOI
69 Richmond, T.J. and Davey, C.A. (2003). The structure of DNA in the nucleosome core. Nature 423, 145-150.   DOI
70 Napoli, A., Zivanovic, Y., Bocs, C., Buhler, C., Rossi, M., Forterre, P., and Ciaramella, M. (2002). DNA bending, compaction and negative supercoiling by the architectural protein Sso7d of Sulfolobus solfataricus. Nucleic Acids Res. 30, 2656-2662.   DOI
71 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.   DOI
72 Smith, S.B., Finzi, L., and Bustamante, C. (1992). Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258, 1122-1126.   DOI
73 Strick, T.R., Allemand, J.F., Bensimon, D., Bensimon, A., and Croquette, V. (1996). The elasticity of a single supercoiled DNA molecule. Science 271, 1835-1837.   DOI
74 Cassina, V., Manghi, M., Salerno, D., Tempestini, A., Iadarola, V., Nardo, L., Brioschi, S., and Mantegazza, F. (2016). Effects of cytosine methylation on DNA morphology: an atomic force microscopy study. Biochim. Biophys. Acta 1860(1 Pt A), 1-7.   DOI
75 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.   DOI
76 Lee, N.K., Kapanidis, A.N., Wang, Y., Michalet, X., Mukhopadhyay, J., Ebright, R.H., and Weiss, S. (2005). Accurate FRET measurements within single diffusing biomolecules using alternating-laser excitation. Biophys. J. 88, 2939-2953.   DOI
77 Satange, R., Chang, C.K., and Hou, M.H. (2018). A survey of recent unusual high-resolution DNA structures provoked by mismatches, repeats and ligand binding. Nucleic Acids Res. 46, 6416-6434.   DOI
78 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.   DOI
79 Tan, C., Terakawa, T., and Takada, S. (2016). Dynamic coupling among protein binding, sliding, and DNA bending revealed by molecular dynamics. J. Am. Chem. Soc. 138, 8512-8522.   DOI
80 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.   DOI
81 Sarangi, M.K., Zvoda, V., Holte, M.N., Becker, N.A., Peters, J.P., Maher, L.J., III, and Ansari, A. (2019). Evidence for a bind-then-bend mechanism for architectural DNA binding protein yNhp6A. Nucleic Acids Res. 47, 2871-2883.   DOI
82 Harrington, R.E. (1993). Studies of DNA bending and flexibility using gel electrophoresis. Electrophoresis 14, 732-746.   DOI
83 Zlatanova, J. and van Holde, K. (2006). Single-molecule biology: what is it and how does it work? Mol. Cell 24, 317-329.   DOI
84 Wang, D.X., Wang, J., Wang, Y.X., Du, Y.C., Huang, Y., Tang, A.N., Cui, Y.X., and Kong, D.M. (2021). DNA nanostructure-based nucleic acid probes: construction and biological applications. Chem. Sci. 12, 7602-7622.   DOI
85 Waters, J.T. and Kim, H.D. (2013). Equilibrium statistics of a surface-pinned semiflexible polymer. Macromolecules 46, 6659-6666.   DOI
86 Yeou, S. and Lee, N.K. (2021). Contribution of a DNA nick to DNA bendability depending on the bending force. Bull. Korean Chem. Soc. 2021 Jul 4 [Epub]. https://doi.org/10.1002/bkcs.12351   DOI
87 van Mameren, J., Gross, P., Farge, G., Hooijman, P., Modesti, M., Falkenberg, M., Wuite, G.J.L., and Peterman, E.J.G. (2009). Unraveling the structure of DNA during overstretching by using multicolor, single-molecule fluorescence imaging. Proc. Natl. Acad. Sci. U. S. A. 106, 18231-18236.   DOI
88 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.   DOI
89 van der Vliet, P.C. and Verrijzer, C.P. (1993). Bending of DNA by transcription factors. Bioessays 15, 25-32.   DOI
90 Vologodskii, A. and Frank-Kamenetskii, M.D. (2013). Strong bending of the DNA double helix. Nucleic Acids Res. 41, 6785-6792.   DOI