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Title: Recovery from slow inactivation in K+ channels is controlled by water molecules

Abstract

Application of a specific stimulus opens the intracellular gate of a K+ channel (activation), yielding a transient period of ion conduction until the selectivity filter spontaneously undergoes a conformational change towards a non-conductive state (inactivation). Removal of the stimulus closes the gate and allows the selectivity filter to interconvert back to its conductive conformation (recovery). Given that the structural differences between the conductive and inactivated filter are very small, it is unclear why the recovery process can take up to several seconds. The bacterial K+ channel KcsA from Streptomyces lividans can be used to help elucidate questions about channel inactivation and recovery at the atomic level. Although KcsA contains only a pore domain, without voltage-sensing machinery, it has the structural elements necessary for ion conduction, activation and inactivation. In this paper we reveal, by means of a series of long molecular dynamics simulations, how the selectivity filter is sterically locked in the inactive conformation by buried water molecules bound behind the selectivity filter. Potential of mean force calculations show how the recovery process is affected by the buried water molecules and the rebinding of an external K+ ion. A kinetic model deduced from the simulations shows how releasing the buriedmore » water molecules can stretch the timescale of recovery to seconds. This leads to the prediction that reducing the occupancy of the buried water molecules by imposing a high osmotic stress should accelerate the rate of recovery, which was verified experimentally by measuring the recovery rate in the presence of a 2-molar sucrose concentration.« less

Authors:
 [1];  [2];  [3];  [1];  [1]
  1. Univ. of Chicago, Chicago, IL (United States). Dept. of Biochemistry and Molecular Biology
  2. Case Western Reserve Univ., Cleveland, OH (United States). School of Medicine, Dept. of Physiology and Biophysics
  3. D.E. Shaw Research, 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:
1564993
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 501; Journal Issue: 7465; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; science & technology

Citation Formats

Ostmeyer, Jared, Chakrapani, Sudha, Pan, Albert C., Perozo, Eduardo, and Roux, Benoît. Recovery from slow inactivation in K+ channels is controlled by water molecules. United States: N. p., 2013. Web. doi:10.1038/nature12395.
Ostmeyer, Jared, Chakrapani, Sudha, Pan, Albert C., Perozo, Eduardo, & Roux, Benoît. Recovery from slow inactivation in K+ channels is controlled by water molecules. United States. https://doi.org/10.1038/nature12395
Ostmeyer, Jared, Chakrapani, Sudha, Pan, Albert C., Perozo, Eduardo, and Roux, Benoît. Sun . "Recovery from slow inactivation in K+ channels is controlled by water molecules". United States. https://doi.org/10.1038/nature12395. https://www.osti.gov/servlets/purl/1564993.
@article{osti_1564993,
title = {Recovery from slow inactivation in K+ channels is controlled by water molecules},
author = {Ostmeyer, Jared and Chakrapani, Sudha and Pan, Albert C. and Perozo, Eduardo and Roux, Benoît},
abstractNote = {Application of a specific stimulus opens the intracellular gate of a K+ channel (activation), yielding a transient period of ion conduction until the selectivity filter spontaneously undergoes a conformational change towards a non-conductive state (inactivation). Removal of the stimulus closes the gate and allows the selectivity filter to interconvert back to its conductive conformation (recovery). Given that the structural differences between the conductive and inactivated filter are very small, it is unclear why the recovery process can take up to several seconds. The bacterial K+ channel KcsA from Streptomyces lividans can be used to help elucidate questions about channel inactivation and recovery at the atomic level. Although KcsA contains only a pore domain, without voltage-sensing machinery, it has the structural elements necessary for ion conduction, activation and inactivation. In this paper we reveal, by means of a series of long molecular dynamics simulations, how the selectivity filter is sterically locked in the inactive conformation by buried water molecules bound behind the selectivity filter. Potential of mean force calculations show how the recovery process is affected by the buried water molecules and the rebinding of an external K+ ion. A kinetic model deduced from the simulations shows how releasing the buried water molecules can stretch the timescale of recovery to seconds. This leads to the prediction that reducing the occupancy of the buried water molecules by imposing a high osmotic stress should accelerate the rate of recovery, which was verified experimentally by measuring the recovery rate in the presence of a 2-molar sucrose concentration.},
doi = {10.1038/nature12395},
journal = {Nature (London)},
number = 7465,
volume = 501,
place = {United States},
year = {Sun Jul 28 00:00:00 EDT 2013},
month = {Sun Jul 28 00:00:00 EDT 2013}
}

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