Conformational Dynamics on the Extracellular Side of LeuT Controlled by Na + and K + Ions and the Protonation State of Glu 290
Abstract
Ions play key mechanistic roles in the gating dynamics of neurotransmitter:sodium symporters (NSSs). In other microsecond scale molecular dynamics simulations of a complete model of the dopamine transporter, a NSS protein, we observed a partitioning of K+ ions from the intracellular side toward the unoccupied Na2 site of dopamine transporter following the release of the Na2-bound Na+. In this work, we evaluate with computational simulations and experimental measurements of ion affinities under corresponding conditions, the consequences of K+ binding in the Na2 site of LeuT, a bacterial homolog of NSS, when both Na+ ions and substrate have left, and the transporter prepares for a new cycle. We compare the results with the consequences of binding Na+ in the same apo system. Analysis of >50-μs atomistic molecular dynamics and enhanced sampling trajectories of constructs with Glu290, either charged or neutral, point to the Glu290 protonation state as a main determinant in the structural reconfiguration of the extracellular vestibule of LeuT in which a “water gate” opens through coordinated motions of residues Leu25, Tyr108, and Phe253. The resulting water channel allows the binding/dissociation of the Na+ and K+ ions that are prevalent, respectively, in the extracellular and intracellular environments.
- Authors:
-
- Cornell Univ., Ithaca, NY (United States)
- Univ. of Copenhagen (Denmark)
- Cornell Univ., Ithaca, NY (United States); National Inst. of Health (NIH), Baltimore, MD (United States)
- Columbia Univ., New York, NY (United States); New York State Psychiatric Inst., New York, NY (United States)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Oak Ridge Leadership Computing Facility (OLCF)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1565483
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of Biological Chemistry
- Additional Journal Information:
- Journal Volume: 291; Journal Issue: 38; Journal ID: ISSN 0021-9258
- Publisher:
- American Society for Biochemistry and Molecular Biology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; conformational change; membrane protein; molecular dynamics; monoamine transporter; neurotransmitter transport
Citation Formats
Khelashvili, George, Schmidt, Solveig Gaarde, Shi, Lei, Javitch, Jonathan A., Gether, Ulrik, Loland, Claus J., and Weinstein, Harel. Conformational Dynamics on the Extracellular Side of LeuT Controlled by Na + and K + Ions and the Protonation State of Glu 290. United States: N. p., 2016.
Web. doi:10.1074/jbc.m116.731455.
Khelashvili, George, Schmidt, Solveig Gaarde, Shi, Lei, Javitch, Jonathan A., Gether, Ulrik, Loland, Claus J., & Weinstein, Harel. Conformational Dynamics on the Extracellular Side of LeuT Controlled by Na + and K + Ions and the Protonation State of Glu 290. United States. https://doi.org/10.1074/jbc.m116.731455
Khelashvili, George, Schmidt, Solveig Gaarde, Shi, Lei, Javitch, Jonathan A., Gether, Ulrik, Loland, Claus J., and Weinstein, Harel. Fri .
"Conformational Dynamics on the Extracellular Side of LeuT Controlled by Na + and K + Ions and the Protonation State of Glu 290". United States. https://doi.org/10.1074/jbc.m116.731455. https://www.osti.gov/servlets/purl/1565483.
@article{osti_1565483,
title = {Conformational Dynamics on the Extracellular Side of LeuT Controlled by Na + and K + Ions and the Protonation State of Glu 290},
author = {Khelashvili, George and Schmidt, Solveig Gaarde and Shi, Lei and Javitch, Jonathan A. and Gether, Ulrik and Loland, Claus J. and Weinstein, Harel},
abstractNote = {Ions play key mechanistic roles in the gating dynamics of neurotransmitter:sodium symporters (NSSs). In other microsecond scale molecular dynamics simulations of a complete model of the dopamine transporter, a NSS protein, we observed a partitioning of K+ ions from the intracellular side toward the unoccupied Na2 site of dopamine transporter following the release of the Na2-bound Na+. In this work, we evaluate with computational simulations and experimental measurements of ion affinities under corresponding conditions, the consequences of K+ binding in the Na2 site of LeuT, a bacterial homolog of NSS, when both Na+ ions and substrate have left, and the transporter prepares for a new cycle. We compare the results with the consequences of binding Na+ in the same apo system. Analysis of >50-μs atomistic molecular dynamics and enhanced sampling trajectories of constructs with Glu290, either charged or neutral, point to the Glu290 protonation state as a main determinant in the structural reconfiguration of the extracellular vestibule of LeuT in which a “water gate” opens through coordinated motions of residues Leu25, Tyr108, and Phe253. The resulting water channel allows the binding/dissociation of the Na+ and K+ ions that are prevalent, respectively, in the extracellular and intracellular environments.},
doi = {10.1074/jbc.m116.731455},
journal = {Journal of Biological Chemistry},
number = 38,
volume = 291,
place = {United States},
year = {Fri Jul 29 00:00:00 EDT 2016},
month = {Fri Jul 29 00:00:00 EDT 2016}
}
Web of Science
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