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Agonist and Antagonist-Diverted Twisting Motions of a Single TRPV1 Channel

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Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Phys. Chem. B 2020, 124, 51, 11617-11624
    B: Biophysics; Physical Chemistry of Biological Systems and Biomolecules

    Agonist and Antagonist-Diverted Twisting Motions of a Single TRPV1 Channel
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    • Shoko Fujimura
      Shoko Fujimura
      AIST-UTokyo Advanced Operando-Measurement Technology Open Innovation Laboratory (OPERANDO-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 6-2-3 Kashiwanoha, Chiba 277-0882, Japan
      More by Shoko Fujimura
      Orcidhttp://orcid.org/0000-0002-0279-5674
    • Kazuhiro Mio*
      Kazuhiro Mio
      AIST-UTokyo Advanced Operando-Measurement Technology Open Innovation Laboratory (OPERANDO-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 6-2-3 Kashiwanoha, Chiba 277-0882, Japan
      Molecular Profiling Research Center for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), Chiba 277-0882, Japan
      *Email: [email protected]
      More by Kazuhiro Mio
    • Masahiro Kuramochi
      Masahiro Kuramochi
      Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Chiba 277-8561, Japan
      AIST-UTokyo Advanced Operando-Measurement Technology Open Innovation Laboratory (OPERANDO-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 6-2-3 Kashiwanoha, Chiba 277-0882, Japan
      More by Masahiro Kuramochi
    • Hiroshi Sekiguchi
      Hiroshi Sekiguchi
      Center for Synchrotron Radiation Research, Japan Synchrotron Radiation Research Institute, 1-1-1 Kouto, Sayo-cho, Hyogo 567-5198, Japan
      More by Hiroshi Sekiguchi
      Orcidhttp://orcid.org/0000-0001-7590-3624
    • Keigo Ikezaki
      Keigo Ikezaki
      Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Chiba 277-8561, Japan
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    • Muneyo Mio
      Muneyo Mio
      AIST-UTokyo Advanced Operando-Measurement Technology Open Innovation Laboratory (OPERANDO-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 6-2-3 Kashiwanoha, Chiba 277-0882, Japan
      Molecular Profiling Research Center for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), 2-3-26 Aomi, Tokyo 135-0064, Japan
      More by Muneyo Mio
    • Kowit Hengphasatporn
      Kowit Hengphasatporn
      Center for Computational Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8577, Japan
      More by Kowit Hengphasatporn
    • Yasuteru Shigeta
      Yasuteru Shigeta
      Center for Computational Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8577, Japan
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      Orcidhttp://orcid.org/0000-0002-3219-6007
    • Tai Kubo
      Tai Kubo
      AIST-UTokyo Advanced Operando-Measurement Technology Open Innovation Laboratory (OPERANDO-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 6-2-3 Kashiwanoha, Chiba 277-0882, Japan
      Molecular Profiling Research Center for Drug Discovery, National Institute of Advanced Industrial Science and Technology (AIST), 2-3-26 Aomi, Tokyo 135-0064, Japan
      More by Tai Kubo
    • Yuji C. Sasaki*
      Yuji C. Sasaki
      Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Chiba 277-8561, Japan
      AIST-UTokyo Advanced Operando-Measurement Technology Open Innovation Laboratory (OPERANDO-OIL), National Institute of Advanced Industrial Science and Technology (AIST), 6-2-3 Kashiwanoha, Chiba 277-0882, Japan
      Center for Synchrotron Radiation Research, Japan Synchrotron Radiation Research Institute, 1-1-1 Kouto, Sayo-cho, Hyogo 567-5198, Japan
      *Email: [email protected]
      More by Yuji C. Sasaki
    Other Access OptionsSupporting Information (3)

    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2020, 124, 51, 11617–11624
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jpcb.0c08250
    Published December 9, 2020
    Copyright © 2020 American Chemical Society
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    Abstract

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    Transient receptor potential vanilloid type 1 (TRPV1) channels are activated by heat, vanilloids, and extracellular protons. Cryo-EM has revealed various conformations of TRPV1, and these structures suggest an intramolecular twisting motion in response to ligand binding. However, limited experimental data support this observation. Here, we analyzed the intramolecular motion of TRPV1 using diffracted X-ray tracking (DXT). DXT analyzes trajectories of Laue spots generated from attached gold nanocrystals and provides picometer spatial and microsecond time scale information about the intramolecular motion. We observed that both an agonist and a competitive antagonist evoked a rotating bias in TRPV1, though these biases were in opposing directions. Furthermore, the rotational bias generated by capsaicin was reversed between the wild-type and the capsaicin-insensitive Y511A mutant. Our findings bolster the understanding of the mechanisms used for activation and modulation of TRP channels, and this knowledge can be exploited for pharmacological usage such as inhibitor design.

    Copyright © 2020 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.0c08250.

    • Video S1: Motion of trajectories classified as long lifetime (MOV)

    • Video S2: Motion of trajectories classified as short lifetime (MOV)

    • Figure S1: Expression and function of TRPV1 receptors used in this experiment; Figure S2: DXT measurement system (upper panels) and the energy profile of incident X-ray for the DXT measurement (lower panel); Figure S3: MSD curves of TRPV1 motion for the χ axis up to 10 ms; Figure S4: VHC provide symmetric distribution for OP-label; Figure S5: Mean-plot of the VSL-label for the further classified short (the lifetime (LT) < 2.5 ms) lifetime group; Figure S6: Subtraction in the probability density between the positive value and the negative value for OP-label at Δt = 0.1 ms; Figure S7: The mean plots of the WT and Y511A against capsaicin for the short lifetime group (LT < 2.0 ms); Figure S8: Superimposed views of closed and open-form of TRPV1; Table S1: Parameter of MSD for wild type of TRPV1; Table S2: Parameter of MSD for each Lifetime group in OP-label with capsaicin (PDF)

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    The Journal of Physical Chemistry B

    Cite this: J. Phys. Chem. B 2020, 124, 51, 11617–11624
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.jpcb.0c08250
    Published December 9, 2020
    Copyright © 2020 American Chemical Society
    Request reuse permissions

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