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High-Sensitivity Detection of Nanometer 1H–19F Distances for Protein Structure Determination by 1H-Detected Fast MAS NMR

Cite this: J. Phys. Chem. B 2019, 123, 20, 4387–4391
Publication Date (Web):April 29, 2019
https://doi.org/10.1021/acs.jpcb.9b03812
Copyright © 2019 American Chemical Society
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    Abstract

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    Protein structure determination by solid-state NMR requires the measurement of many interatomic distances through dipole–dipole couplings. To obtain multiple long-range distance restraints rapidly and with high sensitivity, here we demonstrate a new 1H-detected fast magic-angle-spinning NMR technique that yields many long distances in a two-dimensional (2D)-resolved fashion. The distances are measured up to ∼15 Å, with an accuracy of better than 10%, between 1H and 19F, two nuclear spins that have the highest gyromagnetic ratios. Exogenous fluorines are sparsely introduced into the aromatic residues of the protein, which is perdeuterated and back-exchanged to give amide protons. This 1H–19F distance experiment, termed 2D heteronuclear single-quantum coherence rotational-echo double-resonance (HSQC-REDOR), is demonstrated on the singly fluorinated model protein, GB1. We extracted 33 distances between 5-19F-Trp43 and backbone amide protons, using 2D spectral series that were measured in less than 3 days. Combining these 1H–19F distance restraints with 13C–19F distances and chemical shifts, we calculated a GB1 structure with a backbone root-mean-square deviation of 1.73 Å from the high-resolution structure. This 1H-detected 1H–19F distance technique promises to provide a highly efficient tool for constraining the three-dimensional structures of proteins and protein–ligand complexes, with not only precise and fast measurements but also access to truly long-range distances.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.9b03812.

    • 1H and 15N chemical shifts of fluorinated and nonfluorinated GB1 (Table S1); measured HN–F distances in 5F-W43 CDN-GB1 (Table S2); GB1 structure calculation statistics (Table S3); comparison of the calculated 10 lowest-energy conformers (Table S4); experimental parameters (Table S5); 2D 1H–15N HSQC spectra (Figure S1); representative 2D 1H–19F HSQC-REDOR spectra (Figure S2); simulated 1H–19F REDOR dephasing curves (Figure S3); measured 1H–19F REDOR dephasing (Figure S4); RMSD between simulated and measured 1H–19F REDOR dephasing (Figure S5); correlation of measured 1H–19F distances (Figure S6); and ensemble of 10 lowest-energy GB1 structures (Figure S7) (PDF)

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