An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations

Developing an understanding of the mechanism of voltage-gated ion channels in molecular terms requires knowledge of the structure of the active and resting conformations. Although the active-state conformation is known from x-ray structures, an atomic resolution structure of a voltage-dependent ion channel in the resting state is not currently available. This has motivated various efforts at using computational modeling methods and molecular dynamics (MD) simulations to provide the missing information. A comparison of recent computational results reveals an emerging consensus on voltage-dependent gating from computational modeling and MD simulations. This progress is highlighted in the broad context of preexisting work about voltage-gated channels.

[1]  Francisco Bezanilla,et al.  Intermediate state trapping of a voltage sensor , 2012, The Journal of general physiology.

[2]  Oliver F. Lange,et al.  Determination of solution structures of proteins up to 40 kDa using CS-Rosetta with sparse NMR data from deuterated samples , 2012, Proceedings of the National Academy of Sciences.

[3]  J. Shepherd,et al.  Climate: More ways to govern geoengineering , 2012, Nature.

[4]  William A. Catterall,et al.  Crystal structure of a voltage-gated sodium channel in two potentially inactivated states , 2012, Nature.

[5]  Jianhua He,et al.  Crystal structure of an orthologue of the NaChBac voltage-gated sodium channel , 2012, Nature.

[6]  D. Tobias,et al.  Microscopic origin of gating current fluctuations in a potassium channel voltage sensor. , 2012, Biophysical journal.

[7]  Petra Fromme,et al.  Improving the accuracy of macromolecular structure refinement at 7 Å resolution. , 2012, Structure.

[8]  William A Catterall,et al.  Voltage‐gated sodium channels at 60: structure, function and pathophysiology , 2012, The Journal of physiology.

[9]  Michael L. Klein,et al.  Molecular Dynamics Simulations of Voltage-Gated Cation Channels: Insights on Voltage-Sensor Domain Function and Modulation , 2012, Front. Pharmacol..

[10]  Björn Wallner,et al.  Tracking a complete voltage-sensor cycle with metal-ion bridges , 2012, Proceedings of the National Academy of Sciences.

[11]  Ron O. Dror,et al.  Mechanism of Voltage Gating in Potassium Channels , 2012, Science.

[12]  Klaus Schulten,et al.  Molecular dynamics investigation of the ω-current in the Kv1.2 voltage sensor domains. , 2012, Biophysical journal.

[13]  David Baker,et al.  Structural basis for gating charge movement in the voltage sensor of a sodium channel , 2011, Proceedings of the National Academy of Sciences.

[14]  Francisco Bezanilla,et al.  In Search of a Consensus Model of the Resting State of a Voltage-Sensing Domain , 2011, Neuron.

[15]  W. Catterall,et al.  Gating charge interactions with the S1 segment during activation of a Na+ channel voltage sensor , 2011, Proceedings of the National Academy of Sciences.

[16]  W. Catterall,et al.  THE CRYSTAL STRUCTURE OF A VOLTAGE-GATED SODIUM CHANNEL , 2011, Nature.

[17]  Randy J. Read,et al.  Improved molecular replacement by density- and energy-guided protein structure optimization , 2011, Nature.

[18]  Werner Treptow,et al.  Intermediate states of the Kv1.2 voltage sensor from atomistic molecular dynamics simulations , 2011, Proceedings of the National Academy of Sciences.

[19]  Berk Hess,et al.  3₁₀-helix conformation facilitates the transition of a voltage sensor S4 segment toward the down state. , 2011, Biophysical journal.

[20]  F. Bezanilla,et al.  Properties of deactivation gating currents in Shaker channels. , 2011, Biophysical journal.

[21]  J. Morais-Cabral,et al.  310 helices in channels and other membrane proteins , 2010, The Journal of general physiology.

[22]  M. Klein,et al.  Effect of sensor domain mutations on the properties of voltage-gated ion channels: molecular dynamics studies of the potassium channel Kv1.2. , 2010, Biophysical journal.

[23]  Jianpeng Ma,et al.  Structure of the full-length Shaker potassium channel Kv1.2 by normal-mode-based X-ray crystallographic refinement , 2010, Proceedings of the National Academy of Sciences.

[24]  Klaus Schulten,et al.  Biophysical Journal, Volume 98 Supporting Material Calculation of the Gating Charge for the Kv1.2 Voltage–activated Potassium Channel , 2022 .

[25]  Kresten Lindorff-Larsen,et al.  Principles of conduction and hydrophobic gating in K+ channels , 2010, Proceedings of the National Academy of Sciences.

[26]  W. Catterall,et al.  Sequential formation of ion pairs during activation of a sodium channel voltage sensor , 2009, Proceedings of the National Academy of Sciences.

[27]  Elizabeth J. Denning,et al.  From the gating charge response to pore domain movement: Initial motions of Kv1.2 dynamics under physiological voltage changes , 2009, Molecular membrane biology.

[28]  M. Nishizawa,et al.  Coupling of S4 helix translocation and S6 gating analyzed by molecular-dynamics simulations of mutated Kv channels. , 2009, Biophysical journal.

[29]  M. Klein,et al.  Initial response of the potassium channel voltage sensor to a transmembrane potential. , 2009, Journal of the American Chemical Society.

[30]  Erik Lindahl,et al.  Conformational Changes and Slow Dynamics through Microsecond Polarized Atomistic Molecular Simulation of an Integral Kv1.2 Ion Channel , 2009, PLoS Comput. Biol..

[31]  F. Bezanilla,et al.  S4-based voltage sensors have three major conformations , 2008, Proceedings of the National Academy of Sciences.

[32]  W. Catterall,et al.  Disulfide locking a sodium channel voltage sensor reveals ion pair formation during activation , 2008, Proceedings of the National Academy of Sciences.

[33]  M. Nishizawa,et al.  Molecular dynamics simulation of Kv channel voltage sensor helix in a lipid membrane with applied electric field. , 2008, Biophysical journal.

[34]  Leonardo G. Trabuco,et al.  Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. , 2008, Structure.

[35]  J. Morais-Cabral,et al.  Structure of the transmembrane regions of a bacterial cyclic nucleotide-regulated channel , 2008, Proceedings of the National Academy of Sciences.

[36]  E. Campbell,et al.  Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment , 2007, Nature.

[37]  Benoît Roux,et al.  Closing In on the Resting State of the Shaker K+ Channel , 2007, Neuron.

[38]  Jianpeng Ma,et al.  Normal-mode refinement of anisotropic thermal parameters for potassium channel KcsA at 3.2 A crystallographic resolution. , 2007, Structure.

[39]  Francisco Bezanilla,et al.  Two atomic constraints unambiguously position the S4 segment relative to S1 and S2 segments in the closed state of Shaker K channel , 2007, Proceedings of the National Academy of Sciences.

[40]  C. Deutsch,et al.  A Trapped Intracellular Cation Modulates K+ Channel Recovery From Slow Inactivation , 2006, The Journal of general physiology.

[41]  David Baker,et al.  Voltage sensor conformations in the open and closed states in ROSETTA structural models of K(+) channels. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Francisco Bezanilla,et al.  Gating charge displacement in voltage-gated ion channels involves limited transmembrane movement , 2005, Nature.

[43]  E. Campbell,et al.  Voltage Sensor of Kv1.2: Structural Basis of Electromechanical Coupling , 2005, Science.

[44]  C. Chipot,et al.  Coupled motions between pore and voltage-sensor domains: a model for Shaker B, a voltage-gated potassium channel. , 2004, Biophysical journal.

[45]  F. Bezanilla,et al.  A proton pore in a potassium channel voltage sensor reveals a focused electric field , 2004, Nature.

[46]  Francisco Bezanilla,et al.  Fast gating in the Shaker K+ channel and the energy landscape of activation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[47]  Youxing Jiang,et al.  The principle of gating charge movement in a voltage-dependent K+ channel , 2003, Nature.

[48]  L. Loew,et al.  A Fluorometric Approach to Local Electric Field Measurements in a Voltage-Gated Ion Channel , 2003, Neuron.

[49]  F. Sigworth,et al.  Electrostatics and the Gating Pore of Shaker Potassium Channels , 2001, The Journal of general physiology.

[50]  Francisco Bezanilla,et al.  Voltage Gating of Shaker K+ Channels , 1998, The Journal of general physiology.

[51]  Fred J. Sigworth,et al.  Activation of Shaker Potassium Channels , 1998, The Journal of general physiology.

[52]  Fred J. Sigworth,et al.  Activation of Shaker Potassium Channels , 1998, The Journal of general physiology.

[53]  F. Bezanilla,et al.  Transitions Near the Open State in Shaker K+-channel: Probing with Temperature , 1996, Neuropharmacology.

[54]  G. Yellen,et al.  Two functionally distinct subsites for the binding of internal blockers to the pore of voltage-activated K+ channels. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Roderick MacKinnon,et al.  Contribution of the S4 Segment to Gating Charge in the Shaker K+ Channel , 1996, Neuron.

[56]  Francisco Bezanilla,et al.  Voltage-Sensing Residues in the S2 and S4 Segments of the Shaker K+ Channel , 1996, Neuron.

[57]  G. Yellen,et al.  Use-Dependent Blockers and Exit Rate of the Last Ion from the Multi-Ion Pore of a K+ Channel , 1996, Science.

[58]  F Bezanilla,et al.  Gating of Shaker K+ channels: II. The components of gating currents and a model of channel activation. , 1994, Biophysical journal.

[59]  F J Sigworth,et al.  Voltage gating of ion channels , 1994, Quarterly Reviews of Biophysics.

[60]  T Hoshi,et al.  Shaker potassium channel gating. III: Evaluation of kinetic models for activation , 1994, The Journal of general physiology.

[61]  M. Tanouye,et al.  The size of gating charge in wild-type and mutant Shaker potassium channels. , 1992, Science.

[62]  Y. Jan,et al.  Alteration of voltage-dependence of Shaker potassium channel by mutations in the S4 sequence , 1991, Nature.

[63]  K Wüthrich,et al.  Comparison of the high-resolution structures of the alpha-amylase inhibitor tendamistat determined by nuclear magnetic resonance in solution and by X-ray diffraction in single crystals. , 1989, Journal of molecular biology.

[64]  William A. Catterall,et al.  Voltage-dependent gating of sodium channels: correlating structure and function , 1986, Trends in Neurosciences.

[65]  H. Guy,et al.  Molecular model of the action potential sodium channel. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[66]  W. Catterall,et al.  Molecular properties of voltage-sensitive sodium channels. , 1986, Annual review of biochemistry.

[67]  C. Armstrong,et al.  Sodium channels and gating currents. , 1981, Physiological reviews.

[68]  J. Moore,et al.  Potassium ion current in the squid giant axon: dynamic characteristic. , 1960, Biophysical journal.