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Predicting Site-Binding Modes of Ions and Water to Nucleic Acids Using Molecular Solvation Theory

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    Predicting Site-Binding Modes of Ions and Water to Nucleic Acids Using Molecular Solvation Theory
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    • George M. Giambaşu
      George M. Giambaşu
      Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, New Brunswick, New Jersey 08901, United States
      More by George M. Giambaşu
      Orcidhttp://orcid.org/0000-0003-0581-8605
    • David A. Case
      David A. Case
      Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, New Brunswick, New Jersey 08901, United States
      More by David A. Case
      Orcidhttp://orcid.org/0000-0003-2314-2346
    • Darrin M. York*
      Darrin M. York
      Department of Chemistry and Chemical Biology, Rutgers, The State University of New Jersey, New Brunswick, New Jersey 08901, United States
      Laboratory for Biomolecular Simulation Research, Rutgers, The State University of New Jersey, New Brunswick, New Jersey 08901, United States
      Center for Integrative Proteomics Research, Rutgers, The State University of New Jersey, New Brunswick, New Jersey 08901, United States
      *[email protected]
      More by Darrin M. York
      Orcidhttp://orcid.org/0000-0002-9193-7055
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    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2019, 141, 6, 2435–2445
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    https://doi.org/10.1021/jacs.8b11474
    Published January 11, 2019
    Copyright © 2019 American Chemical Society
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    Abstract

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    Site binding of ions and water shapes nucleic acids folding, dynamics, and biological function, complementing the more diffuse, nonspecific “territorial” ion binding. Unlike territorial binding, prediction of site-specific binding to nucleic acids remains an unsolved challenge in computational biophysics. This work presents a new toolset based on the 3D-RISM molecular solvation theory and topological analysis that predicts cation and water site binding to nucleic acids. 3D-RISM is shown to accurately capture alkali cations and water binding to the central channel, transversal loops, and grooves of the Oxytricha nova’s telomeres’ G-quadruplex (Oxy-GQ), in agreement with high-resolution crystallographic data. To improve the computed cation occupancy along the Oxy-GQ central channel, it was necessary to refine and validate new cation–oxygen parameters using structural and thermodynamic data available for crown ethers and ion channels. This single set of parameters that describes both localized and delocalized binding to various biological systems is used to gain insight into cation occupancy along the Oxy-GQ channel under various salt conditions. The paper concludes with prospects for extending the method to predict divalent cation binding to nucleic acids. This work advances the forefront of theoretical methods able to provide predictive insight into ion atmosphere effects on nucleic acids function.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/jacs.8b11474.

    • List of X-ray structures used in the current work; details on the force field parametrization; description and analysis of NLPB calculations and MD simulations of Oxy-GQ; analysis of 3D-RISM energy minimization of Oxy-GQ X-ray and NMR ensembles; comparison between ion-counting profiles for a 24 bp DNA duplex obtained with the updated force field against recent ion-counting measurements; Figures S1–S6; Tables S1 and S2 (PDF)

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    Cite this: J. Am. Chem. Soc. 2019, 141, 6, 2435–2445
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jacs.8b11474
    Published January 11, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

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