Conformational heterogeneity in closed and open states of the KcsA potassium channel in lipid bicelles

Kim, Dorothy M.; Dikiy, Igor; Upadhyay, Vikrant; Posson, David J.; Eliezer, David; Nimigean, Crina M.

doi:10.1085/jgp.201611602

Title: Conformational heterogeneity in closed and open states of the KcsA potassium channel in lipid bicelles

Journal Article · 18 July 2016 · Journal of General Physiology

DOI: https://doi.org/10.1085/jgp.201611602 · OSTI ID:1625215

Kim, Dorothy M. ^[1]; Dikiy, Igor ^[1]; Upadhyay, Vikrant ^[1]; Posson, David J. ^[1]; Eliezer, David ^[1]; Nimigean, Crina M. ^[1]

Weill Cornell Medical College, New York, NY (United States)

The process of ion channel gating—opening and closing—involves local and global structural changes in the channel in response to external stimuli. Conformational changes depend on the energetic landscape that underlies the transition between closed and open states, which plays a key role in ion channel gating. For the prokaryotic, pH-gated potassium channel KcsA, closed and open states have been extensively studied using structural and functional methods, but the dynamics within each of these functional states as well as the transition between them is not as well understood. In this study, we used solution nuclear magnetic resonance (NMR) spectroscopy to investigate the conformational transitions within specific functional states of KcsA. We incorporated KcsA channels into lipid bicelles and stabilized them into a closed state by using either phosphatidylcholine lipids, known to favor the closed channel, or mutations designed to trap the channel shut by disulfide cross-linking. A distinct state, consistent with an open channel, was uncovered by the addition of cardiolipin lipids. Using selective amino acid labeling at locations within the channel that are known to move during gating, we observed at least two different slowly interconverting conformational states for both closed and open channels. The pH dependence of these conformations and the predictable disruptions to this dependence observed in mutant channels with altered pH sensing highlight the importance of conformational heterogeneity for KcsA gating.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); National Institute of General Medical Sciences (NIGMS); New York State Foundation for Science, Technology, and Innovation (NYSTAR)

Grant/Contract Number:: AC02-76SF00515; RO1GM088352; RO1GM088352-S1; R37AG019391

OSTI ID:: 1625215

Journal Information:: Journal of General Physiology, Vol. 148, Issue 2; ISSN 0022-1295

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 15 works

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References (87)

Reconstitution of integral membrane proteins into isotropic bicelles with improved sample stability and expanded lipid composition profile Morrison, Emma A.; Henzler-Wildman, Katherine A. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1818, Issue 3 https://doi.org/10.1016/j.bbamem.2011.12.020	journal	March 2012
A structural link between inactivation and block of a K+ channel Ader, Christian; Schneider, Robert; Hornig, Sönke Nature Structural & Molecular Biology, Vol. 15, Issue 6 https://doi.org/10.1038/nsmb.1430	journal	May 2008
A quantitative description of membrane current and its application to conduction and excitation in nerve Hodgkin, A. L.; Huxley, A. F. Bulletin of Mathematical Biology, Vol. 52, Issue 1-2 https://doi.org/10.1007/bf02459568	journal	January 1990
Conformational dynamics of the KcsA potassium channel governs gating properties Baker, Kent A.; Tzitzilonis, Christos; Kwiatkowski, Witek Nature Structural & Molecular Biology, Vol. 14, Issue 11 https://doi.org/10.1038/nsmb1311	journal	October 2007
A molecular mechanism for proton-dependent gating in KcsA Cuello, Luis G.; Cortes, D. Marien; Jogini, Vishwanath FEBS Letters, Vol. 584, Issue 6 https://doi.org/10.1016/j.febslet.2010.02.003	journal	February 2010
The Interfacial Lipid Binding Site on the Potassium Channel KcsA Is Specific for Anionic Phospholipids Marius, Phedra; Alvis, Simon J.; East, J. Malcolm Biophysical Journal, Vol. 89, Issue 6 https://doi.org/10.1529/biophysj.105.070755	journal	December 2005
Amphipathic antenna of an inward rectifier K+ channel responds to changes in the inner membrane leaflet Iwamoto, M.; Oiki, S. Proceedings of the National Academy of Sciences, Vol. 110, Issue 2 https://doi.org/10.1073/pnas.1217323110	journal	December 2012
Transmembrane allosteric coupling of the gates in a potassium channel Wylie, B. J.; Bhate, M. P.; McDermott, A. E. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1319577110	journal	December 2013
Structural mechanism of C-type inactivation in K+ channels Cuello, Luis G.; Jogini, Vishwanath; Cortes, D. Marien Nature, Vol. 466, Issue 7303 https://doi.org/10.1038/nature09153	journal	July 2010
Local and global structure of the monomeric subunit of the potassium channel KcsA probed by NMR Chill, Jordan H.; Louis, John M.; Delaglio, Frank Biological Magnetic Resonance Bank https://doi.org/10.13018/bmr7428	dataset	January 2008
pH-Dependent Gating in the Streptomyces lividans K ⁺ Channel ^† Cuello, Luis G.; Romero, Jesus G.; Cortes, D. Marien Biochemistry, Vol. 37, Issue 10 https://doi.org/10.1021/bi972997x	journal	March 1998
Specificity of proteolysis: B. Keil, Springer-Verlag; Heidelberg, 1992; ix + 336 pages; DM 258.00. ISBN 3-540-53118-1 Kay, John FEBS Letters, Vol. 331, Issue 1-2 https://doi.org/10.1016/0014-5793(93)80331-n	journal	September 1993
NMR study of the tetrameric KcsA potassium channel in detergent micelles Chill, J. H. Protein Science, Vol. 15, Issue 4 https://doi.org/10.1110/ps.051954706	journal	March 2006
PHENIX : building new software for automated crystallographic structure determination Adams, Paul D.; Grosse-Kunstleve, Ralf W.; Hung, Li-Wei Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 11 https://doi.org/10.1107/S0907444902016657	journal	October 2002
Probing the Energy Landscape of Activation Gating of the Bacterial Potassium Channel KcsA Linder, Tobias; de Groot, Bert L.; Stary-Weinzinger, Anna PLoS Computational Biology, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pcbi.1003058	journal	May 2013
Functional Equilibrium of the KcsA Structure Revealed by NMR Imai, Shunsuke; Osawa, Masanori; Mita, Kenichiro Journal of Biological Chemistry, Vol. 287, Issue 47 https://doi.org/10.1074/jbc.M112.401265	journal	September 2012
Molecular mechanism of pH sensing in KcsA potassium channels Thompson, A. N.; Posson, D. J.; Parsa, P. V. Proceedings of the National Academy of Sciences, Vol. 105, Issue 19 https://doi.org/10.1073/pnas.0800873105	journal	April 2008
Mechanism for selectivity-inactivation coupling in KcsA potassium channels Cheng, W. W. L.; McCoy, J. G.; Thompson, A. N. Proceedings of the National Academy of Sciences, Vol. 108, Issue 13 https://doi.org/10.1073/pnas.1014186108	journal	March 2011
Inactivation of the Potassium Conductance and Related Phenomena Caused by Quaternary Ammonium Ion Injection in Squid Axons Armstrong, Clay M. The Journal of General Physiology, Vol. 54, Issue 5 https://doi.org/10.1085/jgp.54.5.553	journal	November 1969
Design and characterization of a constitutively open KcsA Cuello, Luis G.; Jogini, Vishwanath; Cortes, D. Marien FEBS Letters, Vol. 584, Issue 6 https://doi.org/10.1016/j.febslet.2010.02.015	journal	February 2010
Gating Mechanism of BK (Slo1) Channels Magleby, Karl L. Journal of General Physiology, Vol. 121, Issue 2 https://doi.org/10.1085/jgp.20028721	journal	January 2003
The Structure of the Potassium Channel: Molecular Basis of K+ Conduction and Selectivity Doyle, D. A. Science, Vol. 280, Issue 5360 https://doi.org/10.1126/science.280.5360.69	journal	April 1998
Structural Rearrangements Underlying K+-Channel Activation Gating Perozo, E. Science, Vol. 285, Issue 5424 https://doi.org/10.1126/science.285.5424.73	journal	July 1999
Mixed modes in opening of KcsA potassium channel from a targeted molecular dynamics simulation Zhong, Wenyu; Guo, Wanlin Biochemical and Biophysical Research Communications, Vol. 388, Issue 1 https://doi.org/10.1016/j.bbrc.2009.07.123	journal	October 2009
Coupling of activation and inactivation gate in a K+-channel: potassium and ligand sensitivity Ader, Christian; Schneider, Robert; Hornig, Sönke The EMBO Journal, Vol. 28, Issue 18 https://doi.org/10.1038/emboj.2009.218	journal	August 2009
Protonation state of E71 in KcsA and its role for channel collapse and inactivation Bhate, M. P.; McDermott, A. E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 38 https://doi.org/10.1073/pnas.1211900109	journal	August 2012
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
Influence of C-Terminal Protein Domains and Protein−Lipid Interactions on Tetramerization and Stability of the Potassium Channel KcsA Molina, M. L.; Encinar, J. A.; Barrera, F. N. Biochemistry, Vol. 43, Issue 47 https://doi.org/10.1021/bi048889+	journal	November 2004
Choosing membrane mimetics for NMR structural studies of transmembrane proteins Warschawski, Dror E.; Arnold, Alexandre A.; Beaugrand, Maïwenn Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1808, Issue 8 https://doi.org/10.1016/j.bbamem.2011.03.016	journal	August 2011
Fluorescence detection of the movement of single KcsA subunits reveals cooperativity Blunck, R.; McGuire, H.; Hyde, H. C. Proceedings of the National Academy of Sciences, Vol. 105, Issue 51 https://doi.org/10.1073/pnas.0807056106	journal	December 2008
Conformational Dynamics at the Inner Gate of KcsA during Activation Hulse, Raymond E.; Sachleben, Joseph R.; Wen, Po-Chao Biochemistry, Vol. 53, Issue 16 https://doi.org/10.1021/bi500168u	journal	April 2014
Lipids in the Structure, Folding, and Function of the KcsA K ⁺ Channel ^† Valiyaveetil, Francis I.; Zhou, Yufeng; MacKinnon, Roderick Biochemistry, Vol. 41, Issue 35 https://doi.org/10.1021/bi026215y	journal	September 2002
Kcsa: It's a Potassium Channel LeMasurier, Meredith; Heginbotham, Lise; Miller, Christopher The Journal of General Physiology, Vol. 118, Issue 3 https://doi.org/10.1085/jgp.118.3.303	journal	August 2001
Local and global structure of the monomeric subunit of the potassium channel KcsA probed by NMR Chill, Jordan H.; Louis, John M.; Delaglio, Frank Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 12 https://doi.org/10.1016/j.bbamem.2007.08.006	journal	December 2007
Mechanism for Selectivity-Inactivation Coupling in KcsA Potassium Channels McCoy, Jason G.; Cheng, Wayland; Thompson, Ameer N. Biophysical Journal, Vol. 100, Issue 3 https://doi.org/10.1016/j.bpj.2010.12.3277	journal	February 2011
Dynamics transitions at the outer vestibule of the KcsA potassium channel during gating Raghuraman, H.; Islam, Shahidul M.; Mukherjee, Soumi Proceedings of the National Academy of Sciences, Vol. 111, Issue 5 https://doi.org/10.1073/pnas.1314875111	journal	January 2014
Chemistry of ion coordination and hydration revealed by a K+ channel–Fab complex at 2.0 Å resolution Zhou, Yufeng; Morais-Cabral, João H.; Kaufman, Amelia Nature, Vol. 414, Issue 6859 https://doi.org/10.1038/35102009	journal	November 2001
Membrane Stiffness and Channel Function ^† Lundbæk, J. A.; Birn, P.; Girshman, J. Biochemistry, Vol. 35, Issue 12 https://doi.org/10.1021/bi952250b	journal	January 1996
Conformational Dynamics in the Selectivity Filter of KcsA in Response to Potassium Ion Concentration Bhate, Manasi P.; Wylie, Benjamin J.; Tian, Lin Journal of Molecular Biology, Vol. 401, Issue 2 https://doi.org/10.1016/j.jmb.2010.06.031	journal	August 2010
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
ANIBAL, Stable Isotope-based Quantitative Proteomics by Aniline and Benzoic Acid Labeling of Amino and Carboxylic Groups Panchaud, Alexandre; Hansson, Jenny; Affolter, Michael Molecular & Cellular Proteomics, Vol. 7, Issue 4 https://doi.org/10.1074/mcp.M700216-MCP200	journal	December 2007
A Quantitative Description of KcsA Gating I: Macroscopic Currents Chakrapani, Sudha; Cordero-Morales, Julio F.; Perozo, Eduardo The Journal of General Physiology, Vol. 130, Issue 5 https://doi.org/10.1085/jgp.200709843	journal	October 2007
Single Streptomyces lividans K+ Channels Heginbotham, Lise; LeMasurier, Meredith; Kolmakova-Partensky, Ludmilla The Journal of General Physiology, Vol. 114, Issue 4 https://doi.org/10.1085/jgp.114.4.551	journal	September 1999
A radioactive uptake assay to measure ion transport across ion channel–containing liposomes Nimigean, Crina M. Nature Protocols, Vol. 1, Issue 3 https://doi.org/10.1038/nprot.2006.166	journal	August 2006
Influence of solubilizing environments on membrane protein structures Cross, Timothy A.; Sharma, Mukesh; Yi, Myunggi Trends in Biochemical Sciences, Vol. 36, Issue 2 https://doi.org/10.1016/j.tibs.2010.07.005	journal	February 2011
A quantitative description of membrane current and its application to conduction and excitation in nerve Hodgkin, A. L.; Huxley, A. F. The Journal of Physiology, Vol. 117, Issue 4 https://doi.org/10.1113/jphysiol.1952.sp004764	journal	August 1952
Molecular interactions involved in proton-dependent gating in KcsA potassium channels Posson, David J.; Thompson, Ameer N.; McCoy, Jason G. The Journal of General Physiology, Vol. 142, Issue 6 https://doi.org/10.1085/jgp.201311057	journal	November 2013
NMRPipe: A multidimensional spectral processing system based on UNIX pipes Delaglio, Frank; Grzesiek, Stephan; Vuister, GeertenW. Journal of Biomolecular NMR, Vol. 6, Issue 3 https://doi.org/10.1007/BF00197809	journal	November 1995
Functional Reconstitution of a Prokaryotic K+ Channel Heginbotham, Lise; Kolmakova-Partensky, Ludmila; Miller, Christopher Journal of General Physiology, Vol. 111, Issue 6 https://doi.org/10.1085/jgp.111.6.741	journal	June 1998
Crystal structure and mechanism of a calcium-gated potassium channel Jiang, Youxing; Lee, Alice; Chen, Jiayun Nature, Vol. 417, Issue 6888 https://doi.org/10.1038/417515a	journal	May 2002
Quantitative Analysis of the Water Occupancy around the Selectivity Filter of a K ⁺ Channel in Different Gating Modes Weingarth, Markus; van der Cruijsen, Elwin A. W.; Ostmeyer, Jared Journal of the American Chemical Society, Vol. 136, Issue 5 https://doi.org/10.1021/ja411450y	journal	January 2014
Molecular determinants of gating at the potassium-channel selectivity filter Cordero-Morales, Julio F.; Cuello, Luis G.; Zhao, Yanxiang Nature Structural & Molecular Biology, Vol. 13, Issue 4 https://doi.org/10.1038/nsmb1069	journal	March 2006
Molecular Architecture of Full-Length KcsA : Role of Cytoplasmic Domains in Ion Permeation and Activation Gating Cortes, D. Marien; Cuello, Luis G.; Perozo, Eduardo The Journal of General Physiology, Vol. 117, Issue 2 https://doi.org/10.1085/jgp.117.2.165	journal	January 2001
Multi-functionality of a tryptophan residue conserved in substrate-binding groove of GH19 chitinases Nagata, Takuya; Shinya, Shoko; Ohnuma, Takayuki Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-81903-3	journal	January 2021
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Local and global structure of the monomeric subunit of the potassium channel KcsA probed by NMR Chill, Jordan H.; Louis, John M.; Delaglio, Frank Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 12 https://doi.org/10.1016/j.bbamem.2007.08.006	journal	December 2007
Mixed modes in opening of KcsA potassium channel from a targeted molecular dynamics simulation Zhong, Wenyu; Guo, Wanlin Biochemical and Biophysical Research Communications, Vol. 388, Issue 1 https://doi.org/10.1016/j.bbrc.2009.07.123	journal	October 2009
Mechanism for Selectivity-Inactivation Coupling in KcsA Potassium Channels McCoy, Jason G.; Cheng, Wayland; Thompson, Ameer N. Biophysical Journal, Vol. 100, Issue 3 https://doi.org/10.1016/j.bpj.2010.12.3277	journal	February 2011
A molecular mechanism for proton-dependent gating in KcsA Cuello, Luis G.; Cortes, D. Marien; Jogini, Vishwanath FEBS Letters, Vol. 584, Issue 6 https://doi.org/10.1016/j.febslet.2010.02.003	journal	February 2010
Design and characterization of a constitutively open KcsA Cuello, Luis G.; Jogini, Vishwanath; Cortes, D. Marien FEBS Letters, Vol. 584, Issue 6 https://doi.org/10.1016/j.febslet.2010.02.015	journal	February 2010
Conformational Dynamics in the Selectivity Filter of KcsA in Response to Potassium Ion Concentration Bhate, Manasi P.; Wylie, Benjamin J.; Tian, Lin Journal of Molecular Biology, Vol. 401, Issue 2 https://doi.org/10.1016/j.jmb.2010.06.031	journal	August 2010
Influence of solubilizing environments on membrane protein structures Cross, Timothy A.; Sharma, Mukesh; Yi, Myunggi Trends in Biochemical Sciences, Vol. 36, Issue 2 https://doi.org/10.1016/j.tibs.2010.07.005	journal	February 2011
Interactions of Anionic Phospholipids and Phosphatidylethanolamine with the Potassium Channel KcsA Alvis, Simon J.; Williamson, Ian M.; East, J. Malcolm Biophysical Journal, Vol. 85, Issue 6 https://doi.org/10.1016/s0006-3495(03)74797-3	journal	December 2003
Influence of C-Terminal Protein Domains and Protein−Lipid Interactions on Tetramerization and Stability of the Potassium Channel KcsA Molina, M. L.; Encinar, J. A.; Barrera, F. N. Biochemistry, Vol. 43, Issue 47 https://doi.org/10.1021/bi048889+	journal	November 2004
Conformational Dynamics at the Inner Gate of KcsA during Activation Hulse, Raymond E.; Sachleben, Joseph R.; Wen, Po-Chao Biochemistry, Vol. 53, Issue 16 https://doi.org/10.1021/bi500168u	journal	April 2014
Membrane Stiffness and Channel Function ^† Lundbæk, J. A.; Birn, P.; Girshman, J. Biochemistry, Vol. 35, Issue 12 https://doi.org/10.1021/bi952250b	journal	January 1996
Quantitative Analysis of the Water Occupancy around the Selectivity Filter of a K ⁺ Channel in Different Gating Modes Weingarth, Markus; van der Cruijsen, Elwin A. W.; Ostmeyer, Jared Journal of the American Chemical Society, Vol. 136, Issue 5 https://doi.org/10.1021/ja411450y	journal	January 2014
Chemistry of ion coordination and hydration revealed by a K+ channel–Fab complex at 2.0 Å resolution Zhou, Yufeng; Morais-Cabral, João H.; Kaufman, Amelia Nature, Vol. 414, Issue 6859 https://doi.org/10.1038/35102009	journal	November 2001
Crystal structure and mechanism of a calcium-gated potassium channel Jiang, Youxing; Lee, Alice; Chen, Jiayun Nature, Vol. 417, Issue 6888 https://doi.org/10.1038/417515a	journal	May 2002
Structural mechanism of C-type inactivation in K+ channels Cuello, Luis G.; Jogini, Vishwanath; Cortes, D. Marien Nature, Vol. 466, Issue 7303 https://doi.org/10.1038/nature09153	journal	July 2010
A structural link between inactivation and block of a K+ channel Ader, Christian; Schneider, Robert; Hornig, Sönke Nature Structural & Molecular Biology, Vol. 15, Issue 6 https://doi.org/10.1038/nsmb.1430	journal	May 2008
Molecular determinants of gating at the potassium-channel selectivity filter Cordero-Morales, Julio F.; Cuello, Luis G.; Zhao, Yanxiang Nature Structural & Molecular Biology, Vol. 13, Issue 4 https://doi.org/10.1038/nsmb1069	journal	March 2006
Conformational dynamics of the KcsA potassium channel governs gating properties Baker, Kent A.; Tzitzilonis, Christos; Kwiatkowski, Witek Nature Structural & Molecular Biology, Vol. 14, Issue 11 https://doi.org/10.1038/nsmb1311	journal	October 2007
Molecular mechanism of pH sensing in KcsA potassium channels Thompson, A. N.; Posson, D. J.; Parsa, P. V. Proceedings of the National Academy of Sciences, Vol. 105, Issue 19 https://doi.org/10.1073/pnas.0800873105	journal	April 2008
Protonation state of E71 in KcsA and its role for channel collapse and inactivation Bhate, M. P.; McDermott, A. E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 38 https://doi.org/10.1073/pnas.1211900109	journal	August 2012
Amphipathic antenna of an inward rectifier K+ channel responds to changes in the inner membrane leaflet Iwamoto, M.; Oiki, S. Proceedings of the National Academy of Sciences, Vol. 110, Issue 2 https://doi.org/10.1073/pnas.1217323110	journal	December 2012
Transmembrane allosteric coupling of the gates in a potassium channel Wylie, B. J.; Bhate, M. P.; McDermott, A. E. Proceedings of the National Academy of Sciences, Vol. 111, Issue 1 https://doi.org/10.1073/pnas.1319577110	journal	December 2013
Identification and Characterization of the Slowly Exchanging pH-dependent Conformational Rearrangement in KcsA Takeuchi, Koh; Takahashi, Hideo; Kawano, Seiko Journal of Biological Chemistry, Vol. 282, Issue 20 https://doi.org/10.1074/jbc.m608264200	journal	March 2007
Molecular Architecture of Full-Length KcsA : Role of Cytoplasmic Domains in Ion Permeation and Activation Gating Cortes, D. Marien; Cuello, Luis G.; Perozo, Eduardo The Journal of General Physiology, Vol. 117, Issue 2 https://doi.org/10.1085/jgp.117.2.165	journal	January 2001
Kcsa: It's a Potassium Channel LeMasurier, Meredith; Heginbotham, Lise; Miller, Christopher The Journal of General Physiology, Vol. 118, Issue 3 https://doi.org/10.1085/jgp.118.3.303	journal	August 2001
A Quantitative Description of KcsA Gating I: Macroscopic Currents Chakrapani, Sudha; Cordero-Morales, Julio F.; Perozo, Eduardo The Journal of General Physiology, Vol. 130, Issue 5 https://doi.org/10.1085/jgp.200709843	journal	October 2007
Molecular interactions involved in proton-dependent gating in KcsA potassium channels Posson, David J.; Thompson, Ameer N.; McCoy, Jason G. The Journal of General Physiology, Vol. 142, Issue 6 https://doi.org/10.1085/jgp.201311057	journal	November 2013
Inactivation of the Potassium Conductance and Related Phenomena Caused by Quaternary Ammonium Ion Injection in Squid Axons Armstrong, Clay M. The Journal of General Physiology, Vol. 54, Issue 5 https://doi.org/10.1085/jgp.54.5.553	journal	November 1969
NMR study of the tetrameric KcsA potassium channel in detergent micelles Chill, J. H. Protein Science, Vol. 15, Issue 4 https://doi.org/10.1110/ps.051954706	journal	March 2006
Structural Rearrangements Underlying K+-Channel Activation Gating Perozo, E. Science, Vol. 285, Issue 5424 https://doi.org/10.1126/science.285.5424.73	journal	July 1999
Probing the Energy Landscape of Activation Gating of the Bacterial Potassium Channel KcsA Linder, Tobias; de Groot, Bert L.; Stary-Weinzinger, Anna PLoS Computational Biology, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pcbi.1003058	journal	May 2013
The Interfacial Lipid Binding Site on the Potassium Channel KcsA Is Specific for Anionic Phospholipids Marius, Phedra; Alvis, Simon J.; East, J. Malcolm Biophysical Journal, Vol. 89, Issue 6 https://doi.org/10.1529/biophysj.105.070755	journal	December 2005

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Rapid constriction of the selectivity filter underlies C-type inactivation in the KcsA potassium channel Li, Jing; Ostmeyer, Jared; Cuello, Luis G. Journal of General Physiology, Vol. 150, Issue 10 https://doi.org/10.1085/jgp.201812082	journal	August 2018
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