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Length-Dependent Melting Kinetics of Short DNA Oligonucleotides Using Temperature-Jump IR Spectroscopy

  • Ryan J. Menssen
    Ryan J. Menssen
    Department of Chemistry, James Franck Institute, and Institute for Biophysical Dynamics, The University of Chicago, 929 East 57th Street, Chicago, Illinois 60637, United States
  •  and 
  • Andrei Tokmakoff*
    Andrei Tokmakoff
    Department of Chemistry, James Franck Institute, and Institute for Biophysical Dynamics, The University of Chicago, 929 East 57th Street, Chicago, Illinois 60637, United States
    *E-mail: [email protected]
Cite this: J. Phys. Chem. B 2019, 123, 4, 756–767
Publication Date (Web):January 7, 2019
https://doi.org/10.1021/acs.jpcb.8b09487
Copyright © 2019 American Chemical Society

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    Abstract

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    In this work, we utilize Fourier transform infrared and temperature-jump (T-jump) infrared (IR) spectroscopy to investigate the melting thermodynamics and kinetics of a series of five DNA sequences ranging from 6 to 14 base pairs long. IR spectroscopy is well suited for the study of DNA because of its ability to distinguish base-specific information, and the nanosecond time resolution of the T-jump apparatus can access the relevant range of kinetics. Eyring analysis of a two-state model examines both the activation enthalpy and entropy, providing new insights into the energetic driving forces and physical processes behind the association and dissociation while also helping to clarify the commonly observed negative activation energy. Global analysis of the thermodynamic and kinetic data applying a linear dependence of activation barriers on oligo length provides a holistic result by producing reasonable agreement between our data and existing nearest-neighbor (NN) thermodynamic parameters blending the experimental results with established predictive models. By studying the trends in the thermodynamics and kinetics as a function of length, this work demonstrates a direct correlation between the effects additional dinucleotides have on the kinetics and the NN parameters for those dinucleotides. This result further supports the development of a kinetic analogue to the thermodynamic NN parameters.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.8b09487.

    • Rate maps for L = 6 and L = 14 demonstrating the fast response that increases with increasing length; Eyring plot comparing the observed rate constants for the adenine and guanine ring modes; Arrhenius analysis fit parameters; Arrhenius plot for the adenine ring mode association and dissociation; association and dissociation activation energies from the literature compared to the results presented here; association and dissociation free-energy of activation as a function of length at multiple temperatures; details of the global fitting method (PDF)

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    16. Kingsley L. Wong, Juewen Liu. Factors and methods to modulate DNA hybridization kinetics. Biotechnology Journal 2021, 16 (11) https://doi.org/10.1002/biot.202000338
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    18. Nick A Rejali, Felix D Ye, Aisha M Zuiter, Caroline C Keller, Carl T Wittwer. Nearest-neighbour transition-state analysis for nucleic acid kinetics. Nucleic Acids Research 2021, 49 (8) , 4574-4585. https://doi.org/10.1093/nar/gkab205
    19. Lin Li, Hongchang Wang, Caiyun Xiong, Di Luo, Hu Chen, Yanhui Liu. Quantify the combined effects of temperature and force on the stability of DNA hairpin. Journal of Physics: Condensed Matter 2021, 33 (18) , 185102. https://doi.org/10.1088/1361-648X/abee38
    20. Takanori Harashima, Yusuke Hasegawa, Satoshi Kaneko, Yuki Jono, Shintaro Fujii, Manabu Kiguchi, Tomoaki Nishino. Elementary processes of DNA surface hybridization resolved by single-molecule kinetics: implication for macroscopic device performance. Chemical Science 2021, 12 (6) , 2217-2224. https://doi.org/10.1039/D0SC04449K
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    22. Romeo C A Dubini, Alexander Schön, Markus Müller, Thomas Carell, Petra Rovó. Impact of 5-formylcytosine on the melting kinetics of DNA by 1H NMR chemical exchange. Nucleic Acids Research 2020, 48 (15) , 8796-8807. https://doi.org/10.1093/nar/gkaa589
    23. N. N. Kurus, F. N. Dultsev, V. M. Golyshev, D. V. Nekrasov, D. V. Pyshnyi, A. A. Lomzov. A QCM-based rupture event scanning technique as a simple and reliable approach to study the kinetics of DNA duplex dissociation. Analytical Methods 2020, 12 (30) , 3771-3777. https://doi.org/10.1039/D0AY00613K
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