The impact of DNA intercalators on DNA and DNA-processing enzymes elucidated through force-dependent binding kinetics

Nature Communications

Volumn 6, Issue , 2015, Pages

  Biebricher, Andreas S ^a   Heller, Iddo ^a   Roijmans, Roel F H ^a   Hoekstra, Tjalle P ^a   Peterman, Erwin J G ^a   Wuite, Gijs J L ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CYANINE DYE; DNA; DNA INTERCALATOR; DNA POLYMERASE; INTERCALATING AGENT; UNCLASSIFIED DRUG; BACTERIOPHAGE T7 INDUCED DNA POLYMERASE; DNA DIRECTED DNA POLYMERASE;

DNA; DYE; ENZYME ACTIVITY; FLUORESCENCE; PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; DISSOCIATION; DNA BINDING; DNA DENATURATION; DNA PROBE; ENTEROBACTERIA PHAGE LAMBDA; ENZYME ACTIVITY; ENZYME BINDING; ENZYME KINETICS; FLUORESCENCE MICROSCOPY; FORCE SPECTROSCOPY; IN VITRO STUDY; INVESTIGATIVE PROCEDURES; IONIC STRENGTH; ISOTHERM; NONHUMAN; OPTICAL TWEEZERS; QUANTITATIVE ANALYSIS; SPECTROSCOPY; CHEMISTRY; KINETICS; KYMOGRAPHY;

DNA; DNA-DIRECTED DNA POLYMERASE; INTERCALATING AGENTS; KINETICS; KYMOGRAPHY;

EID: 84935036158     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8304     Document Type: Article

References (52)

1. Lerman, L. S. Structural considerations in the interaction of DNA and acridines. J. Mol. Biol. 3, 18-IN14 (1961).
2. Glazer, A. N. & Rye, H. S. Stable dye-DNA intercalation complexes as reagents for high-sensitivity fluorescence detection. Nature 359, 859-861 (1992).
3. Perkins, T. T. Single polymer dynamics in an elongational flow. Science 276, 2016-2021 (1997).
4. Glazer, A. N., Peck, K. & Mathies, R. A. A stable double-stranded DNAethidium homodimer complex: application to picogram fluorescence detection of DNA in agarose gels. Proc. Natl Acad. Sci. USA 87, 3851-3855 (1990).
5. Bianco, P. R. et al. Processive translocation and DNA unwinding by individual RecBCD enzyme molecules. Nature 409, 374-378 (2001).
6. Finkelstein, I. J., Visnapuu, M.-L. & Greene, E. C. Single-molecule imaging reveals mechanisms of protein disruption by a DNA translocase. Nature 468, 983-987 (2010).
7. Hamdan, S. M., Loparo, J. J., Takahashi, M., Richardson, C. C. & van Oijen, A. M. Dynamics of DNA replication loops reveal temporal control of laggingstrand synthesis. Nature 457, 336-339 (2009).
8. Hurley, L. H. DNA and its associated processes as targets for cancer therapy. Nat. Rev. Cancer 2, 188-200 (2002).
9. Koster, D. A., Palle, K., Bot, E. S. M., Bjornsti, M.-A. & Dekker, N. H. Antitumour drugs impede DNA uncoiling by topoisomerase I. Nature 448, 213-217 (2007).
10. Paramanathan, T., Vladescu, I., McCauley, M. J., Rouzina, I. & Williams, M. C. Force spectroscopy reveals the DNA structural dynamics that govern the slow binding of Actinomycin D. Nucleic Acids Res. 40, 4925-4932 (2012).
11. Reuter, M., Parry, F., Dryden, D. T. F. & Blakely, G. W. Single-molecule imaging of Bacteroides fragilis AddAB reveals the highly processive translocation of a single motor helicase. Nucleic Acids Res. 38, 3721-3731 (2010).
12. Vladescu, I. D., McCauley, M. J., Nuñez, M. E., Rouzina, I. & Williams, M. C. Quantifying force-dependent and zero-force DNA intercalation by singlemolecule stretching. Nat. Methods 4, 517-522 (2007).
13. Smith, S., Finzi, L. & Bustamante, C. Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258, 1122-1126 (1992).
14. Murade, C. U., Subramaniam, V., Otto, C. & Bennink, M. L. Interaction of oxazole yellow dyes with DNA studied with hybrid optical tweezers and fluorescence microscopy. Biophys. J. 97, 835-843 (2009).
15. Paik, D. H. & Perkins, T. T. Dynamics and multiple stable binding modes of DNA intercalators revealed by single-molecule force spectroscopy. Angew. Chem. Int. Ed. 51, 1811-1815 (2012).
16. Günther, K., Mertig, M., Seidel, R. & Gu, K. Mechanical and structural properties of YOYO-1 complexed DNA. Nucleic Acids Res. 38, 6526-6532 (2010).
17. Sischka, A. et al. Molecular mechanisms and kinetics between DNA and DNA binding ligands. Biophys. J. 88, 404-411 (2005).
18. Rocha, M. S., Ferreira, M. C. & Mesquita, O. N. Transition on the entropic elasticity of DNA induced by intercalating molecules. J. Chem. Phys. 127, 105108 (2007).
19. Lerman, L. The structure of the DNA-acridine complex. Proc. Natl Acad. Sci. USA 49, 94-102 (1963).
20. Tsai, C., Jain, S. & Sobell, H. X-ray crystallographic visualization of drugnucleic acid intercalative binding: structure of an ethidium-dinucleoside monophosphate crystalline complex, Ethidium: 5-iodouridylyl (3'-5') adenosine. Proc. Natl Acad. Sci. USA 72, 628-632 (1975).
21. Wang, A. H., Ughetto, G., Quigley, G. J. & Rich, A. Interactions between an anthracycline antibiotic and DNA: molecular structure of daunomycin complexed to d(CpGpTpApCpG) at 1.2-A resolution. Biochemistry 26, 1152-1163 (1987).
22. Gao, Q. et al. Drug-induced DNA repair: X-ray structure of a DNAditercalinium complex. Proc. Natl Acad. Sci. USA 88, 2422-2426 (1991).
23. Ughetto, G. et al. A comparison of the structure of echinomycin and triostin A complexed to a DNA fragment. Nucleic Acids Res. 13, 2305-2323 (1985).
24. Ihmels, H. & Otto, D. in Supermolecular Dye Chem. Vol. 258 (ed Würthner, F.) 161-204 (Springer Berlin Heidelberg, 2005).
25. Yan, X. et al. Probing the kinetics of SYTOX Orange stain binding to doublestranded DNA with implications for DNA analysis. Anal. Chem. 77, 3554-3562 (2005).
26. Van Mameren, J. et al. Counting RAD51 proteins disassembling from nucleoprotein filaments under tension. Nature 457, 745-748 (2009).
27. Candelli, A., Wuite, G. J. L. & Peterman, E. J. G. Combining optical trapping, fluorescence microscopy and micro-fluidics for single molecule studies of DNA-protein interactions. Phys. Chem. Chem. Phys. 13, 7263-7272 (2011).
28. Heller, I. et al. STED nanoscopy combined with optical tweezers reveals protein dynamics on densely covered DNA. Nat. Methods 10, 910-916 (2013).
29. Heller, I., Hoekstra, T. P., King, G. A., Peterman, E. J. G. & Wuite, G. J. L. Optical tweezers analysis of DNA-protein complexes. Chem. Rev. 114, 3087-3119 (2014).
30. Gross, P., Farge, G., Peterman, E. J. G. & Wuite, G. J. L. Combining optical tweezers, single-molecule fluorescence microscopy, and microfluidics for studies of DNA-protein interactions. Methods Enzymol. 475, 427-453 (2010).
31. Hayashi, M. & Harada, Y. Direct observation of the reversible unwinding of a single DNA molecule caused by the intercalation of ethidium bromide. Nucleic Acids Res. 35, e125 (2007).
32. McGhee, J. D. & von Hippel, P. H. Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J. Mol. Biol. 86, 469-489 (1974).
33. Nyberg, L., Persson, F., Akerman, B. & Westerlund, F. Heterogeneous staining: a tool for studies of how fluorescent dyes affect the physical properties of DNA. Nucleic Acids Res. 41, e184 (2013).
34. Wilson, W. D., Krishnamoorthy, C. R., Wang, Y. H. & Smith, J. C. Mechanism of intercalation: ion effects on the equilibrium and kinetic constants for the interaction of propidium and ethidium with DNA. Biopolymers 24, 1941-1961 (1985).
35. King, G. A. et al. Revealing the competition between peeled ssDNA, melting bubbles, and S-DNA during DNA overstretching using fluorescence microscopy. Proc. Natl Acad. Sci. USA 110, 3859-3864 (2013).
36. Wuite, G. J., Smith, S. B., Young, M., Keller, D. & Bustamante, C. Singlemolecule studies of the effect of template tension on T7 DNA polymerase activity. Nature 404, 103-106 (2000).
37. Candelli, A. et al. A toolbox for generating single-stranded DNA in optical tweezers experiments. Biopolymers 99, 611-620 (2013).
38. Hammond, G. S. A correlation of reaction rates. J. Am. Chem. Soc. 77, 334-338 (1955).
39. Leffler, J. E. Parameters for the description of transition states. Science 117, 340-341 (1953).
40. Hopkins, H. P., Stevenson, K. A. & Wilson, W. D. Enthalpy and entropy changes for the intercalation of small molecules to DNA. I. Substituted naphthalene monoimides and naphthalene diimides. J. Solution Chem. 15, 563-579 (1986).
41. Hopkins, H. P., Ming, Y., Wilson, W. D. & Boykin, D. W. Intercalation binding of 6-substituted naphthothiopheneamides to DNA: enthalpy and entropy components. Biopolymers 31, 1105-1114 (1991).
42. Schwaller, M. A., Dodin, G. & Aubard, J. Thermodynamics of drug-DNA interactions: entropy-driven intercalation and enthalpy-driven outside binding in the ellipticine series. Biopolymers 31, 519-527 (1991).
43. Wilson, W. D. & Lopp, I. G. Analysis of cooperativity and ion effects in the interaction of quinacrine with DNA. Biopolymers 18, 3025-3041 (1979).
44. Petty, J. T., Bordelon, J. A. & Robertson, M. E. Thermodynamic characterization of the association of cyanine dyes with DNA. J. Phys. Chem. B 104, 7221-7227 (2000).
45. Larsson, A., Carlsson, C., Jonsson, M. & Albinsson, B. Characterization of the binding of the fluorescent dyes YO and YOYO to DNA by polarized light spectroscopy. J. Am. Chem. Soc. 116, 8459-8465 (1994).
46. Vladescu, I., McCauley, M., Rouzina, I. & Williams, M. Mapping the phase diagram of single DNA molecule force-induced melting in the presence of ethidium. Phys. Rev. Lett. 95, 158102 (2005).
47. Biebricher, A. et al. PICH: a DNA translocase specially adapted for processing anaphase bridge DNA. Mol. Cell 51, 691-701 (2013).
48. Van Mameren, J. et al. Unraveling the structure of DNA during overstretching by using multicolor, single-molecule fluorescence imaging. Proc. Natl Acad. Sci. USA 106, 18231-18236 (2009).
49. Heller, I. et al. Mobility analysis of super-resolved proteins on optically stretched DNA: comparing imaging techniques and parameters. Chem Phys. Chem. 15, 727-733 (2014).
50. Gittes, F. & Schmidt, C. F. Interference model for back-focal-plane displacement detection in optical tweezers. Opt. Lett. 23, 7-9 (1998).
51. Johnson, I. D. The Molecular Probes Handbook: A Guide to Fluorescent Probes and Labeling Technologies 11th edn. (Life Technologies Corporation, 2010).
52. Dimeric Cyanine Nucleic Acids Stains. https://tools.lifetechnologies.com/ content/sfs/manuals/mp03600.pdf (2001).