Invincible DNA tethers: Covalent DNA anchoring for enhanced temporal and force stability in magnetic tweezers experiments

Nucleic Acids Research

Volumn 42, Issue 18, 2014, Pages e137-

  Janissen, Richard ^a   Berghuis, Bojk A ^a   Dulin, David ^a   Wink, Max ^a   Van Laar, Theo ^a   Dekker, Nynke H ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; MACROGOL DERIVATIVE;

BIOMECHANICS; CHEMISTRY; MAGNET; SPECTROSCOPY;

BIOMECHANICAL PHENOMENA; DNA; MAGNETS; POLYETHYLENE GLYCOLS; SPECTRUM ANALYSIS;

EID: 84922392459     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku677     Document Type: Article

References (60)

1. Greenleaf,W. J., Woodside,M. T. and Block,S. M. (2007) High-resolution, single-molecule measurements of biomolecular motion. Annu. Rev. Biophys. Biomol. Struct., 36, 171-190.
2. Dulin,D., Lipfert,J., Moolman,M. C. and Dekker,N. H. (2013) Studying genomic processes at the single-molecule level: introducing the tools and applications. Nat. Rev. Genet., 14, 9-22.
3. Neuman,K. C. and Nagy,A. (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods, 5, 491-505.
4. Fazal,F. M. and Block,S. M. (2011) Optical tweezers study life under tension. Nat. Photonics, 5, 318-321.
5. Janssen,X. J., Lipfert,J., Jager,T., Daudey,R., Beekman,J. and Dekker,N. H. (2012) Electromagnetic torque tweezers: a versatile approach for measurement of single-molecule twist and torque. Nano Lett., 12, 3634-3639.
6. La Porta,A. and Wang,M. D. (2004) Optical torque wrench: angular trapping, rotation, and torque detection of quartz microparticles. Phy. Rev. Lett., 92, 190801-1-190801-4.
7. Lipfert,J., Kerssemakers,J. W., Jager,T. and Dekker,N. H. (2010) Magnetic torque tweezers: measuring torsional stiffness in DNA and RecA-DNA filaments. Nat. Methods, 7, 977-980.
8. De Vlaminck,I., Henighan,T., van Loenhout,M. T. J., Burnham,D. R. and Dekker,C. (2012) Magnetic forces and DNA mechanics in multiplexed magnetic tweezers. PLoS One, 7, e41432.
9. Lipfert,J., Koster,D. A., Vilfan,I. D., Hage,S. and Dekker,N. H. (2009) Single-molecule magnetic tweezers studies of type IB topoisomerases. Methods Mol. Biol., 582, 71-89.
10. Ribeck,N. and Saleh,O. A. (2008) Multiplexed single-molecule measurements with magnetic tweezers. Rev. Sci. Instrum., 79, 094301-094306.
11. Woodside,M. T., Behnke-Parks,W. M., Larizadeh,K., Travers,K., Herschlag,D. and Block,S. M. (2006) Nanomechanical measurements of the sequence-dependent folding landscapes of single nucleic acid hairpins. Proc. Natl. Acad. Sci. U. S. A., 103, 6190-6195.
12. Zhou,J., Schweikhard,V. and Block,S. M. (2013) Single-molecule studies of RNAPII elongation. Biochim. Biophys. Acta, 1829, 29-38.
13. Dobrovolskaia,I. V. and Arya,G. (2012) Dynamics of forced nucleosome unraveling and role of nonuniform histone-DNA interactions. Biophys. J., 103, 989-998.
14. Rico,F., Gonzalez,L., Casuso,I., Puig-Vidal,M. and Scheuring,S. (2013) High-speed force spectroscopy unfolds titin at the velocity of molecular dynamics simulations. Science, 342, 741-743.
15. Herrero-Galan,E., Fuentes-Perez,M. E., Carrasco,C., Valpuesta,J. M., Carrascosa,J. L., Moreno-Herrero,F. and Arias-Gonzalez,J. R. (2013) Mechanical identities of RNA and DNA double helices unveiled at the single-molecule level. J. Am. Chem. Soc., 135, 122-131.
16. Smith,D. E., Tans,S. J., Smith,S. B., Grimes,S., Anderson,D. L. and Bustamante,C. (2001) The bacteriophage straight phi29 portal motor can package DNA against a large internal force. Nature, 413, 748-752.
17. Bongini,L., Melli,L., Lombardi,V. and Bianco,P. (2014) Transient kinetics measured with force steps discriminate between double-stranded DNA elongation and melting and define the reaction energetics. Nucleic Acids Res., 42, 3436-3449.
18. Bell,G. I. (1978) Models for the specific adhesion of cells to cells. Science, 200, 618-627.
19. Evans,E. (2001) Probing the relation between force-lifetime-and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct., 30, 105-128.
20. Evans,E. and Ritchie,K. (1997) Dynamic strength of molecular adhesion bonds. Biophys. J., 72, 1541-1555.
21. Lipfert,J., Wiggin,M., Kerssemakers,J. W., Pedaci,F. and Dekker,N. H. (2011) Freely orbiting magnetic tweezers to directly monitor changes in the twist of nucleic acids. Nat. Commun., 2, 439-448.
22. 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.
23. 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.
24. 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. U. S. A., 94, 6185-6190.
25. Neuert,G., Albrecht,C., Pamir,E. and Gaub,H. E. (2006) Dynamic force spectroscopy of the digoxigenin-antibody complex. FEBS Lett., 580, 505-509.
26. de Odrowaz Piramowicz,M., Czuba,P., Targosz,M., Burda,K. and Szymonski,M. (2006) Dynamic force measurements of avidin-biotin and streptavdin-biotin interactions using AFM. Acta Biochim. Pol., 53, 93-100.
27. Friddle,R. W., Noy,A. and De Yoreo,J. J. (2012) Interpreting the widespread nonlinear force spectra of intermolecular bonds. Proc. Natl. Acad. Sci. U. S. A., 109, 13573-13578.
28. Janissen,R., Oberbarnscheidt,L. and Oesterhelt,F. (2009) Optimized straight forward procedure for covalent surface immobilization of different biomolecules for single molecule applications. Colloids Surf. B. Biointerfaces, 71, 200-207.
29. Janissen,R. and Oesterhelt,F. (2010) Directed deposition of single molecules on surfaces. J. Nanosci. Nanotechnol., 10, 5328-5332.
30. Bentzen,E. L., Tomlinson,I. D.,Mason,J., Gresch,P., Warnement,M. R.,Wright,D., Sanders-Bush,E., Blakely,R. and Rosenthal,S. J. (2005) Surface modification to reduce nonspecific binding of quantum dots in live cell assays. Bioconjug. Chem., 16, 1488-1494.
31. Puchner,E. M. and Gaub,H. E. (2009) Force and function: probing proteins with AFM-based force spectroscopy. Curr. Opin. Struct. Biol., 19, 605-614.
32. Ho,D., Falter,K., Severin,P. and Gaub,H. E. (2009) DNA as a force sensor in an aptamer-based biochip for adenosine. Anal. Chem., 81, 3159-3164.
33. Yang,Z., Galloway,J. A. and Yu,H. (1999) Protein interactions with poly(ethylene glycol) self-assembled monolayers on glass substrates: diffusion and adsorption. Langmuir, 15, 8405-8411.
34. Rodriguez-Emmenegger,C., Brynda,E., Riedel,T., Houska,M., Subr,V., Alles,A. B., Hasan,E., Gautrot,J. E. and Huck,W. T. (2011) Polymer brushes showing non-fouling in blood plasma challenge the currently accepted design of protein resistant surfaces. Macromol. Rapid Commun., 32, 952-957.
35. Chan,R. T. H.,Marçal,H., Russell,R. A., Holden,P. J. and Foster,L. J. R. (2011) Application of polyethylene glycol to promote cellular biocompatibility of polyhydroxybutyrate films. Int. J. Polym. Sci., 2011, 473045-1-473045-9.
36. Alcantar,N. A., Aydil,E. S. and Israelachvili,J. N. (2000) Polyethylene glycol-coated biocompatible surfaces. J. Biomed. Mater. Res., 51, 343-351.
37. Upadhyayula,S., Quinata,T., Bishop,S., Gupta,S., Johnson,N. R., Bahmani,B., Bozhilov,K., Stubbs,J., Jreij,P., Nallagatla,P. et al. (2012) Coatings of polyethylene glycol for suppressing adhesion between solid microspheres and flat surfaces. Langmuir, 28, 5059-5069.
38. Jain,A., Liu,R., Xiang,Y. K. and Ha,T. (2012) Single-molecule pull-down for studying protein interactions. Nat. Protoc., 7, 445-452.
39. Crut,A., Nair,P. A., Koster,D. A., Shuman,S. and Dekker,N. H. (2008) Dynamics of phosphodiester synthesis by DNA ligase. Proc. Natl. Acad. Sci. U. S. A., 105, 6894-6899.
40. Games,P. A., Keselman,H. J. and Rogan,J. C. (1983) A review of simultaneous painvise multiple comparisons. Stat. Neerl., 37, 53-58.
41. te Velthuis,A. J., Kerssemakers,J. W., Lipfert,J. and Dekker,N. H. (2010) Quantitative guidelines for force calibration through spectral analysis of magnetic tweezers data. Biophys. J., 99, 1292-1302.
42. Charvin,G., Vologodskii,A., Bensimon,D. and Croquette,V. (2005) Braiding DNA: experiments, simulations, and models. Biophys. J., 88, 4124-4136.
43. Sweryda-Krawiec,B., Devaraj,H., Jacob,G. and Hickman,J. J. (2004) A new interpretation of serum albumin surface passivation. Langmuir, 20, 2054-2056.
44. Israelachvili,J. (2005) Differences between non-specific and bio-specific, and between equilibrium and non-equilibrium, interactions in biological systems. Q. Rev. Biophys., 38, 331-337.
45. Leckband,D. and Israelachvili,J. (2001) Intermolecular forces in biology. Q. Rev. Biophys., 34, 105-267.
46. Vilfan,I. D., Lipfert,J., Koster,D. A., Lemay,S. G. and Dekker,N. H. (2009) Magnetic tweezers for single-molecule experiments. In Hinterdorfer,P. and van Oijen,A. (eds.), Handbook of Single-Molecule Biophysics. Springer-Verlag, New York, pp. 371-395.
47. Kruithof,M., Chien,F., de Jager,M. and van Noort,J. (2008) Subpiconewton dynamic force spectroscopy using magnetic tweezers. Biophys. J., 94, 2343-2348.
48. Czerwinski,F., Richardson,A. C. and Oddershede,L. B. (2009) Quantifying noise in optical tweezers by allan variance. Opt. Express, 17, 13255-13269.
49. Kim,K. and Saleh,O. A. (2009) A high-resolution magnetic tweezer for single-molecule measurements. Nucleic Acids Res., 37, e136.
50. 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.
51. Cluzel,P., Lebrun,A., Heller,C., Lavery,R., Viovy,J. L., Chatenay,D. and Caron,F. (1996) DNA: an extensible molecule. Science, 271, 792-794.
52. Manosas,M., Meglio,A., Spiering,M. M., Ding,F., Benkovic,S. J., Barre,F. X., Saleh,O. A., Allemand,J. F., Bensimon,D. and Croquette,V. (2010) Magnetic tweezers for the study of DNA tracking motors. Methods Enzymol., 475, 297-320.
53. Tarsa,P. B., Brau,R. R., Barch,M., Ferrer,J. M., Freyzon,Y., Matsudaira,P. and Lang,M. J. (2007) Detecting Force-Induced Molecular Transitions with Fluorescence Resonant Energy Transfer. Angewandte Chemie, International Edition, 46, 1999-2001.
54. Odijk,T. (1977) Polyelectrolytes near the rod limit. Journal ofPolym er Science: Polymer Physics Edition, 15, 477-483.
55. Wang,M. D., Yin,H., Landick,R., Gelles,J. and Block,S. M. (1997) Stretching DNA with optical tweezers. Biophys. J., 72, 1335-1346.
56. Bosco,A., Camunas-Soler,J. and Ritort,F. (2014) Elastic properties and secondary structure formation of single-stranded DNA at monovalent and divalent salt conditions. Nucleic Acids Res., 42, 2064-2074.
57. 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.
58. Grandbois,M., Beyer,M., Rief,M., Clausen-Schaumann,H. and Gaub,H. E. (1999) How strong is a covalent bond? Science, 283, 1727-1730.
59. Yuan,C., Chen,A., Kolb,P. and Moy,V. T. (2000) Energy landscape of streptavidin-biotin complexes measured by atomic force microscopy. Biochemistry, 39, 10219-10223.
60. Zheng,P., Cao,Y. and Li,H. (2011) Facile method of constructing polyproteins for single-molecule force spectroscopy studies. Langmuir, 27, 5713-5718.