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Conformational Ensembles of an Intrinsically Disordered Protein Consistent with NMR, SAXS, and Single-Molecule FRET

  • Gregory-Neal W. Gomes*
    Gregory-Neal W. Gomes
    Department of Physics, University of Toronto, Toronto, Ontario M5G 1X8, Canada
    Department of Chemical and Physical Sciences, University of Toronto Mississauga, Mississauga, Ontario L5L 1C6, Canada
    *Email: [email protected]
  • Mickaël Krzeminski
    Mickaël Krzeminski
    Molecular Medicine Program, Hospital for Sick Children, Toronto, Ontario M5S 1A8, Canada
    Department of Biochemistry, University of Toronto, Toronto, Ontario M5G 1X8, Canada
  • Ashley Namini
    Ashley Namini
    Department of Physics, University of Toronto, Toronto, Ontario M5G 1X8, Canada
    Department of Chemical and Physical Sciences, University of Toronto Mississauga, Mississauga, Ontario L5L 1C6, Canada
  • Erik W. Martin
    Erik W. Martin
    Department of Structural Biology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, United States
  • Tanja Mittag
    Tanja Mittag
    Department of Structural Biology, St. Jude Children’s Research Hospital, Memphis, Tennessee 38105, United States
    More by Tanja Mittag
  • Teresa Head-Gordon
    Teresa Head-Gordon
    Departments of Chemistry, Bioengineering, Chemical and Biomolecular Engineering University of California, Berkeley, California 94720, United States
  • Julie D. Forman-Kay
    Julie D. Forman-Kay
    Molecular Medicine Program, Hospital for Sick Children, Toronto, Ontario M5S 1A8, Canada
    Department of Biochemistry, University of Toronto, Toronto, Ontario M5G 1X8, Canada
  • , and 
  • Claudiu C. Gradinaru*
    Claudiu C. Gradinaru
    Department of Physics, University of Toronto, Toronto, Ontario M5G 1X8, Canada
    Department of Chemical and Physical Sciences, University of Toronto Mississauga, Mississauga, Ontario L5L 1C6, Canada
    *Email: [email protected]
Cite this: J. Am. Chem. Soc. 2020, 142, 37, 15697–15710
Publication Date (Web):August 25, 2020
https://doi.org/10.1021/jacs.0c02088
Copyright © 2020 American Chemical Society

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    Abstract

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    Intrinsically disordered proteins (IDPs) have fluctuating heterogeneous conformations, which makes their structural characterization challenging. Although challenging, characterization of the conformational ensembles of IDPs is of great interest, since their conformational ensembles are the link between their sequences and functions. An accurate description of IDP conformational ensembles depends crucially on the amount and quality of the experimental data, how it is integrated, and if it supports a consistent structural picture. We used integrative modeling and validation to apply conformational restraints and assess agreement with the most common structural techniques for IDPs: Nuclear Magnetic Resonance (NMR) spectroscopy, Small-angle X-ray Scattering (SAXS), and single-molecule Förster Resonance Energy Transfer (smFRET). Agreement with such a diverse set of experimental data suggests that details of the generated ensembles can now be examined with a high degree of confidence. Using the disordered N-terminal region of the Sic1 protein as a test case, we examined relationships between average global polymeric descriptions and higher-moments of their distributions. To resolve apparent discrepancies between smFRET and SAXS inferences, we integrated SAXS data with NMR data and reserved the smFRET data for independent validation. Consistency with smFRET, which was not guaranteed a priori, indicates that, globally, the perturbative effects of NMR or smFRET labels on the Sic1 ensemble are minimal. Analysis of the ensembles revealed distinguishing features of Sic1, such as overall compactness and large end-to-end distance fluctuations, which are consistent with biophysical models of Sic1’s ultrasensitive binding to its partner Cdc4. Our results underscore the importance of integrative modeling and validation in generating and drawing conclusions from IDP conformational ensembles.

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    • Extended description of smFRET and SAXS experiment/analysis, ENSEMBLE methods, and additional tables (PDF)

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