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Unfolded-State Dynamics and Structure of Protein L Characterized by Simulation and Experiment

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Department of Chemistry, Stanford University, Stanford, California 94305, Department of Physics and Astronomy, Michigan State University, East Lansing, Michigan 48824, and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan 48824
†Stanford University.
‡Department of Physics and Astronomy, Michigan State University.
§Department of Biochemistry and Molecular Biology, Michigan State University.
Cite this: J. Am. Chem. Soc. 2010, 132, 13, 4702–4709
Publication Date (Web):March 10, 2010
https://doi.org/10.1021/ja908369h
Copyright © 2010 American Chemical Society

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    Abstract

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    While several experimental techniques now exist for characterizing protein unfolded states, all-atom simulation of unfolded states has been challenging due to the long time scales and conformational sampling required. We address this problem by using a combination of accelerated calculations on graphics processor units and distributed computing to simulate tens of thousands of molecular dynamics trajectories each up to ∼10 μs (for a total aggregate simulation time of 127 ms). We used this approach in conjunction with Trp-Cys contact quenching experiments to characterize the unfolded structure and dynamics of protein L. We employed a polymer theory method to make quantitative comparisons between high-temperature simulated and chemically denatured experimental ensembles and find that reaction-limited quenching rates calculated from simulation agree remarkably well with experiment. In both experiment and simulation, we find that unfolded-state intramolecular diffusion rates are very slow compared to highly denatured chains and that a single-residue mutation can significantly alter unfolded-state dynamics and structure. This work suggests a view of the unfolded state in which surprisingly low diffusion rates could limit folding and opens the door for all-atom molecular simulation to be a useful predictive tool for characterizing protein unfolded states along with experiments that directly measure intramolecular diffusion.

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    Figures S1−S8; Table S1; detailed descriptions of GPU and CPU simulation methods, Trp-Cys quenching experimental materials and methods; methods for calibrating simulated unfolded ensembles with experiment. This material is available free of charge via the Internet at http://pubs.acs.org.

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