Characterization of conformational equilibria through Hamiltonian replica-exchange simulations: Prevailing over large energy barriers, close confinement and strong entropic and solvation effects

COMP 109

José D. Faraldo-Gómez, faraldo@uchicago.edu and Benoît Roux. Institute for Molecular Pediatric Sciences, University of Chicago, Center for Integrative Sciences, 929 East 57th Street, Chicago, IL 60637
Simulations based on the replica-exchange molecular-dynamics framework (REMD) are emerging as a useful tool to describe the conformational variability that is intrinsic to most chemical and biological systems. We show that a novel extension of this method, known as Hamiltonian REMD, greatly facilitates the characterization of conformational equilibria across large energetic barriers, or in the presence of substantial entropic effects, overcoming some of the difficulties of temperature-based REMD. In particular, we compare HREMD and TREMD through computation of the gas-phase free-energy difference between the D2d and S4 states of tetrabutylammonium (TBA), an important compound in ion-channel physiology. Taking advantage of the greater efficiency of the HREMD scheme, the conformational equilibrium of TBA was investigated in a variety of conditions. Simulation of the gas-phase equilibrium in the 100-300 K range allowed us to determine the entropy difference between these states, as well as its temperature dependence. Through HREMD simulations in a water droplet, the effect of solvation on the equilibrium was also elucidated. Finally, TBA was simulated within the binding cavity of the KcsA potassium channel, and density maps for the protein-ligand complex were constructed and compared with X-ray crystallography data. Novel insights were thus gained into the association of potassium channels with quaternary-ammonium blockers such as TBA, specifically in relation to the energetic coupling with permeant ions. Overall, this work illustrates the potential of HREMD in the context of molecular recognition and computational drug design, in which one of the most challenging issues remains to account for conformational flexibility.