Long Lifetime of Hydrogen-Bonded DNA Basepairs by Force Spectroscopy

Fuhrmann A, Getfert S, Fu Q, Reimann P, Lindsay S, Ros R (2012)
Biophysical Journal 102(10): 2381-2390.

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Abstract
Electron-tunneling data suggest that a noncovalently-bonded complex of three molecules, two recognition molecules that present hydrogen-bond donor and acceptor sites via a carboxamide group, and a DNA base, remains bound for seconds. This is surprising, given that imino-proton exchange rates show that basepairs in a DNA double helix open on millisecond timescales. The long lifetime of the three-molecule complex was confirmed using force spectroscopy, but measurements on DNA basepairs are required to establish a comparison with the proton-exchange data. Here, we report on a dynamic force spectroscopy study of complexes between the bases adenine and thymine (A-T, two-hydrogen bonds) and 2-aminoadenine and thymine (2AA-T, three-hydrogen bonds). Bases were tethered to an AFM probe and mica substrate via long, covalently linked polymer tethers. Data for bond-survival probability versus force and the rupture-force distributions were well fitted by the Bell model. The resulting lifetime of the complexes at zero pulling force was similar to 2 s for two-hydrogen bonds (A-T) and similar to 4 s for three-hydrogen bonds (2AA-T). Thus, DNA basepairs in an AFM pulling experiment remain bonded for long times, even without the stabilizing influence of base-stacking in a double helix. This result suggests that the pathways for opening, and perhaps the open states themselves, are very different in the AFM and proton-exchange measurements.
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Fuhrmann A, Getfert S, Fu Q, Reimann P, Lindsay S, Ros R. Long Lifetime of Hydrogen-Bonded DNA Basepairs by Force Spectroscopy. Biophysical Journal. 2012;102(10):2381-2390.
Fuhrmann, A., Getfert, S., Fu, Q., Reimann, P., Lindsay, S., & Ros, R. (2012). Long Lifetime of Hydrogen-Bonded DNA Basepairs by Force Spectroscopy. Biophysical Journal, 102(10), 2381-2390.
Fuhrmann, A., Getfert, S., Fu, Q., Reimann, P., Lindsay, S., and Ros, R. (2012). Long Lifetime of Hydrogen-Bonded DNA Basepairs by Force Spectroscopy. Biophysical Journal 102, 2381-2390.
Fuhrmann, A., et al., 2012. Long Lifetime of Hydrogen-Bonded DNA Basepairs by Force Spectroscopy. Biophysical Journal, 102(10), p 2381-2390.
A. Fuhrmann, et al., “Long Lifetime of Hydrogen-Bonded DNA Basepairs by Force Spectroscopy”, Biophysical Journal, vol. 102, 2012, pp. 2381-2390.
Fuhrmann, A., Getfert, S., Fu, Q., Reimann, P., Lindsay, S., Ros, R.: Long Lifetime of Hydrogen-Bonded DNA Basepairs by Force Spectroscopy. Biophysical Journal. 102, 2381-2390 (2012).
Fuhrmann, Alexander, Getfert, Sebastian, Fu, Qiang, Reimann, Peter, Lindsay, Stuart, and Ros, Robert. “Long Lifetime of Hydrogen-Bonded DNA Basepairs by Force Spectroscopy”. Biophysical Journal 102.10 (2012): 2381-2390.
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6 Citations in Europe PMC

Data provided by Europe PubMed Central.

Resolving the molecular mechanism of cadherin catch bond formation.
Manibog K, Li H, Rakshit S, Sivasankar S., Nat Commun 5(), 2014
PMID: 24887573
Single-molecule spectroscopy of amino acids and peptides by recognition tunnelling.
Zhao Y, Ashcroft B, Zhang P, Liu H, Sen S, Song W, Im J, Gyarfas B, Manna S, Biswas S, Borges C, Lindsay S., Nat Nanotechnol 9(6), 2014
PMID: 24705512
Different roles of cadherins in the assembly and structural integrity of the desmosome complex.
Lowndes M, Rakshit S, Shafraz O, Borghi N, Harmon RM, Green KJ, Sivasankar S, Nelson WJ., J. Cell. Sci. 127(Pt 10), 2014
PMID: 24610950

49 References

Data provided by Europe PubMed Central.

Theoretical analysis of single-molecule force spectroscopy experiments: heterogeneity of chemical bonds.
Raible M, Evstigneev M, Bartels FW, Eckel R, Nguyen-Duong M, Merkel R, Ros R, Anselmetti D, Reimann P., Biophys. J. 90(11), 2006
PMID: 16513778
Quantitative analysis of single-molecule RNA-protein interaction.
Fuhrmann A, Schoening JC, Anselmetti D, Staiger D, Ros R., Biophys. J. 96(12), 2009
PMID: 19527663
Antibody-unfolding and metastable-state binding in force spectroscopy and recognition imaging.
Kaur P, Qiang-Fu , Fuhrmann A, Ros R, Kutner LO, Schneeweis LA, Navoa R, Steger K, Xie L, Yonan C, Abraham R, Grace MJ, Lindsay S., Biophys. J. 100(1), 2011
PMID: 21190677
Detection and localization of individual antibody-antigen recognition events by atomic force microscopy.
Hinterdorfer P, Baumgartner W, Gruber HJ, Schilcher K, Schindler H., Proc. Natl. Acad. Sci. U.S.A. 93(8), 1996
PMID: 8622961
Antigen binding forces of individually addressed single-chain Fv antibody molecules.
Ros R, Schwesinger F, Anselmetti D, Kubon M, Schafer R, Pluckthun A, Tiefenauer L., Proc. Natl. Acad. Sci. U.S.A. 95(13), 1998
PMID: 9636161
Single molecule force spectroscopy by AFM indicates helical structure of poly(ethylene-glycol) in water
Oesterhelt F., Rief M., Gaub H.E.., 1999
Strength of multiple parallel biological bonds.
Sulchek T, Friddle RW, Noy A., Biophys. J. 90(12), 2006
PMID: 16581843
Dynamic force spectroscopy of single DNA molecules.
Strunz T, Oroszlan K, Schafer R, Guntherodt HJ., Proc. Natl. Acad. Sci. U.S.A. 96(20), 1999
PMID: 10500167
Direct measurements of base stacking interactions in DNA by single-molecule atomic-force spectroscopy.
Ke C, Humeniuk M, S-Gracz H, Marszalek PE., Phys. Rev. Lett. 99(1), 2007
PMID: 17678193
Unzipping DNA oligomers
Krautbauer R., Rief M., Gaub H.E.., 2003
Dynamic force spectroscopy: Analysis of reversible bond-breaking dynamics.
Diezemann G, Janshoff A., J Chem Phys 129(8), 2008
PMID: 19044850
Stretching and rupturing individual supramolecular polymer chains by AFM.
Zou S, Schonherr H, Vancso GJ., Angew. Chem. Int. Ed. Engl. 44(6), 2005
PMID: 15624231
Extracting kinetics from single-molecule force spectroscopy: nanopore unzipping of DNA hairpins.
Dudko OK, Mathe J, Szabo A, Meller A, Hummer G., Biophys. J. 92(12), 2007
PMID: 17384066
Analyzing single-bond experiments: influence of the shape of the energy landscape and universal law between the width, depth, and force spectrum of the bond
Husson J., Pincet F.., 2008
Supramolecular chemistry at the single-molecule level.
Eckel R, Ros R, Decker B, Mattay J, Anselmetti D., Angew. Chem. Int. Ed. Engl. 44(3), 2005
PMID: 15624136
Unbinding forces of single antibody-antigen complexes correlate with their thermal dissociation rates.
Schwesinger F, Ros R, Strunz T, Anselmetti D, Guntherodt HJ, Honegger A, Jermutus L, Tiefenauer L, Pluckthun A., Proc. Natl. Acad. Sci. U.S.A. 97(18), 2000
PMID: 10963664
Affinity-matured recombinant antibody fragments analyzed by single-molecule force spectroscopy.
Morfill J, Blank K, Zahnd C, Luginbuhl B, Kuhner F, Gottschalk KE, Pluckthun A, Gaub HE., Biophys. J. 93(10), 2007
PMID: 17675348
Recognition force spectroscopy studies of the NTA-His bond
Kienberger F., Kada G., Hinterdorfer P.., 2000
Effector-stimulated single molecule protein-DNA interactions of a quorum-sensing system in Sinorhizobium meliloti.
Bartels FW, McIntosh M, Fuhrmann A, Metzendorf C, Plattner P, Sewald N, Anselmetti D, Ros R, Becker A., Biophys. J. 92(12), 2007
PMID: 17384071
Single molecule recognition between cytochrome C 551 and gold-immobilized azurin by force spectroscopy.
Bonanni B, Kamruzzahan AS, Bizzarri AR, Rankl C, Gruber HJ, Hinterdorfer P, Cannistraro S., Biophys. J. 89(4), 2005
PMID: 16192283
On the detection of single bond ruptures in dynamic force spectroscopy by AFM.
Karacsony O, Akhremitchev BB., Langmuir 27(18), 2011
PMID: 21838324
Hidden multiple bond effects in dynamic force spectroscopy.
Getfert S, Reimann P., Biophys. J. 102(5), 2012
PMID: 22404941

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