Voltage profile along the permeation pathway of an open channel

Jorge E. Contreras, Jin Chen, Albert Y Lau, Vishwanath Jogini, Benoît Roux, Miguel Holmgren

Research output: Contribution to journalArticle

Abstract

For ion channels, the transmembrane potential plays a critical role by acting as a driving force for permeant ions. At the microscopic level, the transmembrane potential is thought to decay nonlinearly across the ion permeation pathway because of the irregular three-dimensional shape of the channel's pore. By taking advantage of the current structural and functional understanding of cyclic nucleotide-gated channels, in this study we experimentally explore the transmembrane potential's distribution across the open pore. As a readout for the voltage drop, we engineered cysteine residues along the selectivity filter and scanned the sensitivity of their modification rates by Ag+ to the transmembrane potential. The experimental data, which indicate that the majority of the electric field drops across the selectivity filter, are in good agreement with continuum electrostatic calculations using a homology model of an open CNG channel. By focusing the transmembrane potential across the selectivity filter, the electromotive driving force is coupled with the movement of permeant ions in the filter, maximizing the efficiency of this process.

Original languageEnglish (US)
Pages (from-to)2863-2869
Number of pages7
JournalBiophysical Journal
Volume99
Issue number9
DOIs
StatePublished - Nov 3 2010
Externally publishedYes

Fingerprint

Membrane Potentials
Ions
Cyclic Nucleotide-Gated Cation Channels
Static Electricity
Ion Channels
Cysteine

ASJC Scopus subject areas

  • Biophysics

Cite this

Contreras, J. E., Chen, J., Lau, A. Y., Jogini, V., Roux, B., & Holmgren, M. (2010). Voltage profile along the permeation pathway of an open channel. Biophysical Journal, 99(9), 2863-2869. https://doi.org/10.1016/j.bpj.2010.08.053

Voltage profile along the permeation pathway of an open channel. / Contreras, Jorge E.; Chen, Jin; Lau, Albert Y; Jogini, Vishwanath; Roux, Benoît; Holmgren, Miguel.

In: Biophysical Journal, Vol. 99, No. 9, 03.11.2010, p. 2863-2869.

Research output: Contribution to journalArticle

Contreras, JE, Chen, J, Lau, AY, Jogini, V, Roux, B & Holmgren, M 2010, 'Voltage profile along the permeation pathway of an open channel', Biophysical Journal, vol. 99, no. 9, pp. 2863-2869. https://doi.org/10.1016/j.bpj.2010.08.053
Contreras, Jorge E. ; Chen, Jin ; Lau, Albert Y ; Jogini, Vishwanath ; Roux, Benoît ; Holmgren, Miguel. / Voltage profile along the permeation pathway of an open channel. In: Biophysical Journal. 2010 ; Vol. 99, No. 9. pp. 2863-2869.
@article{75163800a67b4835b138a6adeafb293e,
title = "Voltage profile along the permeation pathway of an open channel",
abstract = "For ion channels, the transmembrane potential plays a critical role by acting as a driving force for permeant ions. At the microscopic level, the transmembrane potential is thought to decay nonlinearly across the ion permeation pathway because of the irregular three-dimensional shape of the channel's pore. By taking advantage of the current structural and functional understanding of cyclic nucleotide-gated channels, in this study we experimentally explore the transmembrane potential's distribution across the open pore. As a readout for the voltage drop, we engineered cysteine residues along the selectivity filter and scanned the sensitivity of their modification rates by Ag+ to the transmembrane potential. The experimental data, which indicate that the majority of the electric field drops across the selectivity filter, are in good agreement with continuum electrostatic calculations using a homology model of an open CNG channel. By focusing the transmembrane potential across the selectivity filter, the electromotive driving force is coupled with the movement of permeant ions in the filter, maximizing the efficiency of this process.",
author = "Contreras, {Jorge E.} and Jin Chen and Lau, {Albert Y} and Vishwanath Jogini and Beno{\^i}t Roux and Miguel Holmgren",
year = "2010",
month = "11",
day = "3",
doi = "10.1016/j.bpj.2010.08.053",
language = "English (US)",
volume = "99",
pages = "2863--2869",
journal = "Biophysical Journal",
issn = "0006-3495",
publisher = "Biophysical Society",
number = "9",

}

TY - JOUR

T1 - Voltage profile along the permeation pathway of an open channel

AU - Contreras, Jorge E.

AU - Chen, Jin

AU - Lau, Albert Y

AU - Jogini, Vishwanath

AU - Roux, Benoît

AU - Holmgren, Miguel

PY - 2010/11/3

Y1 - 2010/11/3

N2 - For ion channels, the transmembrane potential plays a critical role by acting as a driving force for permeant ions. At the microscopic level, the transmembrane potential is thought to decay nonlinearly across the ion permeation pathway because of the irregular three-dimensional shape of the channel's pore. By taking advantage of the current structural and functional understanding of cyclic nucleotide-gated channels, in this study we experimentally explore the transmembrane potential's distribution across the open pore. As a readout for the voltage drop, we engineered cysteine residues along the selectivity filter and scanned the sensitivity of their modification rates by Ag+ to the transmembrane potential. The experimental data, which indicate that the majority of the electric field drops across the selectivity filter, are in good agreement with continuum electrostatic calculations using a homology model of an open CNG channel. By focusing the transmembrane potential across the selectivity filter, the electromotive driving force is coupled with the movement of permeant ions in the filter, maximizing the efficiency of this process.

AB - For ion channels, the transmembrane potential plays a critical role by acting as a driving force for permeant ions. At the microscopic level, the transmembrane potential is thought to decay nonlinearly across the ion permeation pathway because of the irregular three-dimensional shape of the channel's pore. By taking advantage of the current structural and functional understanding of cyclic nucleotide-gated channels, in this study we experimentally explore the transmembrane potential's distribution across the open pore. As a readout for the voltage drop, we engineered cysteine residues along the selectivity filter and scanned the sensitivity of their modification rates by Ag+ to the transmembrane potential. The experimental data, which indicate that the majority of the electric field drops across the selectivity filter, are in good agreement with continuum electrostatic calculations using a homology model of an open CNG channel. By focusing the transmembrane potential across the selectivity filter, the electromotive driving force is coupled with the movement of permeant ions in the filter, maximizing the efficiency of this process.

UR - http://www.scopus.com/inward/record.url?scp=78349289288&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=78349289288&partnerID=8YFLogxK

U2 - 10.1016/j.bpj.2010.08.053

DO - 10.1016/j.bpj.2010.08.053

M3 - Article

C2 - 21044583

AN - SCOPUS:78349289288

VL - 99

SP - 2863

EP - 2869

JO - Biophysical Journal

JF - Biophysical Journal

SN - 0006-3495

IS - 9

ER -