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AggFluor: Fluorogenic Toolbox Enables Direct Visualization of the Multi-Step Protein Aggregation Process in Live Cells

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    AggFluor: Fluorogenic Toolbox Enables Direct Visualization of the Multi-Step Protein Aggregation Process in Live Cells
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    • Charles H. Wolstenholme
      Charles H. Wolstenholme
      Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
      More by Charles H. Wolstenholme
    • Hang Hu
      Hang Hu
      Department of Chemistry  and  Molecular Engineering and Sciences Institute, University of Washington, Seattle, Washington 98105, United States
      More by Hang Hu
    • Songtao Ye
      Songtao Ye
      Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
      More by Songtao Ye
    • Brian E. Funk
      Brian E. Funk
      Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
      More by Brian E. Funk
    • Divya Jain
      Divya Jain
      Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
      More by Divya Jain
    • Chia-Heng Hsiung
      Chia-Heng Hsiung
      Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
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    • Gang Ning
      Gang Ning
      The Huck Institute of Life Sciences, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
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    • Yu Liu*
      Yu Liu
      Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
      *[email protected]
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    • Xiaosong Li*
      Xiaosong Li
      Department of Chemistry, University of Washington, Seattle, Washington 98105, United States
      *[email protected]
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      Orcidhttp://orcid.org/0000-0001-7341-6240
    • Xin Zhang*
      Xin Zhang
      Department of Chemistry,  Department of Biochemistry and Molecular Biology  and  The Huck Institute of Life Sciences, The Pennsylvania State University, University Park, Pennsylvania 16802, United States
      *[email protected]
      More by Xin Zhang
      Orcidhttp://orcid.org/0000-0001-6686-1645
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    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2020, 142, 41, 17515–17523
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    https://doi.org/10.1021/jacs.0c07245
    Published September 11, 2020
    Copyright © 2020 American Chemical Society
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    Abstract

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    Aberrantly processed or mutant proteins misfold and assemble into a variety of soluble oligomers and insoluble aggregates, a process that is associated with an increasing number of diseases that are not curable or manageable. Herein, we present a chemical toolbox, AggFluor, that allows for live cell imaging and differentiation of complex aggregated conformations in live cells. Based on the chromophore core of green fluorescent proteins, AggFluor is comprised of a series of molecular rotor fluorophores that span a wide range of viscosity sensitivity. As a result, these compounds exhibit differential turn-on fluorescence when incorporated in either soluble oligomers or insoluble aggregates. This feature allows us to develop, for the first time, a dual-color imaging strategy to distinguish unfolded protein oligomers from insoluble aggregates in live cells. Furthermore, we have demonstrated how small molecule proteostasis regulators can drive formation and disassembly of protein aggregates in both conformational states. In summary, AggFluor is the first set of rationally designed molecular rotor fluorophores that evenly cover a wide range of viscosity sensitivities. This set of fluorescent probes not only change the status quo of current imaging methods to visualize protein aggregation in live cells but also can be generally applied to study other biological processes that involve local viscosity changes with temporal and spatial resolutions.

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