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Trajectory-Based Simulation of EPR Spectra: Models of Rotational Motion for Spin Labels on Proteins

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    Trajectory-Based Simulation of EPR Spectra: Models of Rotational Motion for Spin Labels on Proteins
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    • Peter D. Martin
      Peter D. Martin
      Department of Biochemistry, Molecular Biology, and Biophysics  and  School of Physics and Astronomy, University of Minnesota, Minneapolis, Minnesota 55455, United States
      More by Peter D. Martin
    • Bengt Svensson
      Bengt Svensson
      Department of Biochemistry, Molecular Biology, and Biophysics, University of Minnesota, Minneapolis, Minnesota 55455, United States
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      Orcidhttp://orcid.org/0000-0003-3932-2376
    • David D. Thomas*
      David D. Thomas
      Department of Biochemistry, Molecular Biology, and Biophysics  and  School of Physics and Astronomy, University of Minnesota, Minneapolis, Minnesota 55455, United States
      *E-mail: [email protected] (D.D.T.). Phone: (612) 626-0957.
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    • Stefan Stoll*
      Stefan Stoll
      Department of Chemistry, University of Washington, Seattle, Washington 98195, United States
      *E-mail: [email protected] (S.S.). Phone: (206) 543-2906.
      More by Stefan Stoll
      Orcidhttp://orcid.org/0000-0003-4255-9550
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    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2019, 123, 48, 10131–10141
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jpcb.9b02693
    Published November 6, 2019
    Copyright © 2019 American Chemical Society
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    Abstract

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    Direct time-domain simulation of continuous-wave (CW) electron paramagnetic resonance (EPR) spectra from molecular dynamics (MD) trajectories has become increasingly popular, especially for proteins labeled with nitroxide spin labels. Due to the time-consuming nature of simulating adequately long MD trajectories, two approximate methods have been developed to reduce the MD-trajectory length required for modeling EPR spectra: hindered Brownian diffusion (HBD) and hidden Markov models (HMMs). Here, we assess the accuracy of these two approximate methods relative to direct simulations from MD trajectories for three spin-labeled protein systems (a simple helical peptide, a soluble protein, and a membrane protein) and two nitroxide spin labels with differing mobilities (R1 and 2,2,6,6-tetramethylpiperidine-1-oxyl-4-amino-4-carboxylic acid (TOAC)). We find that the HMMs generally outperform HBD. Although R1 dynamics partially resembles hindered Brownian diffusion, HMMs accommodate the multiple dynamic time scales for the transitions between rotameric states of R1 that cannot be captured accurately by a HBD model. The MD trajectories of the TOAC-labeled proteins show that its dynamics closely resembles slow multisite exchange between twist-boat and chair ring puckering states. This motion is modeled well by HMM but not by HBD. All MD-trajectory data processing, stochastic trajectory simulations, and CW EPR spectral simulations are implemented in EasySpin, a free software package for MATLAB.

    Copyright © 2019 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.jpcb.9b02693.

    • Conversion formulas between different rotation representations, expressions of the orientational potential using Wigner D-matrices and quaternions, MD simulation parameters, details on processing MD simulation results, plots of all dihedral trajectories, validation of time-domain CW EPR spectral simulations against a frequency-domain (SLE) solver, m3 results for the R1-labeled systems, and mm results for TOAC-polyalanine (PDF)

    • TOAC force field parameters (ZIP)

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    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

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    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2019, 123, 48, 10131–10141
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jpcb.9b02693
    Published November 6, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

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