CryoEM structures of Kv1.2 potassium channels, conducting and non-conducting

We present near-atomic-resolution cryoEM structures of the mammalian voltage-gated potassium channel Kv1.2 in open, C-type inactivated, toxin-blocked and sodium-bound states at 3.2 Å, 2.5 Å, 3.2 Å, and 2.9 Å. These structures, all obtained at nominally zero membrane potential in detergent micelles,...

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Main Authors: Yangyu Wu, Yangyang Yan, Youshan Yang, Shumin Bian, Alberto Rivetta, Ken Allen, Fred J Sigworth
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-02-01
Series:eLife
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Online Access:https://elifesciences.org/articles/89459
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author Yangyu Wu
Yangyang Yan
Youshan Yang
Shumin Bian
Alberto Rivetta
Ken Allen
Fred J Sigworth
author_facet Yangyu Wu
Yangyang Yan
Youshan Yang
Shumin Bian
Alberto Rivetta
Ken Allen
Fred J Sigworth
author_sort Yangyu Wu
collection DOAJ
description We present near-atomic-resolution cryoEM structures of the mammalian voltage-gated potassium channel Kv1.2 in open, C-type inactivated, toxin-blocked and sodium-bound states at 3.2 Å, 2.5 Å, 3.2 Å, and 2.9 Å. These structures, all obtained at nominally zero membrane potential in detergent micelles, reveal distinct ion-occupancy patterns in the selectivity filter. The first two structures are very similar to those reported in the related Shaker channel and the much-studied Kv1.2–2.1 chimeric channel. On the other hand, two new structures show unexpected patterns of ion occupancy. First, the toxin α-Dendrotoxin, like Charybdotoxin, is seen to attach to the negatively-charged channel outer mouth, and a lysine residue penetrates into the selectivity filter, with the terminal amine coordinated by carbonyls, partially disrupting the outermost ion-binding site. In the remainder of the filter two densities of bound ions are observed, rather than three as observed with other toxin-blocked Kv channels. Second, a structure of Kv1.2 in Na+ solution does not show collapse or destabilization of the selectivity filter, but instead shows an intact selectivity filter with ion density in each binding site. We also attempted to image the C-type inactivated Kv1.2 W366F channel in Na+ solution, but the protein conformation was seen to be highly variable and only a low-resolution structure could be obtained. These findings present new insights into the stability of the selectivity filter and the mechanism of toxin block of this intensively studied, voltage-gated potassium channel.
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spelling doaj-art-aaa5389f848742a3aca08545de6158bd2025-08-20T02:13:41ZengeLife Sciences Publications LtdeLife2050-084X2025-02-011210.7554/eLife.89459CryoEM structures of Kv1.2 potassium channels, conducting and non-conductingYangyu Wu0https://orcid.org/0000-0001-8064-6132Yangyang Yan1Youshan Yang2Shumin Bian3Alberto Rivetta4Ken Allen5Fred J Sigworth6https://orcid.org/0000-0002-7178-8494Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, United StatesDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, United StatesDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, United StatesDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, United StatesDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, United StatesDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, United StatesDepartment of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, United StatesWe present near-atomic-resolution cryoEM structures of the mammalian voltage-gated potassium channel Kv1.2 in open, C-type inactivated, toxin-blocked and sodium-bound states at 3.2 Å, 2.5 Å, 3.2 Å, and 2.9 Å. These structures, all obtained at nominally zero membrane potential in detergent micelles, reveal distinct ion-occupancy patterns in the selectivity filter. The first two structures are very similar to those reported in the related Shaker channel and the much-studied Kv1.2–2.1 chimeric channel. On the other hand, two new structures show unexpected patterns of ion occupancy. First, the toxin α-Dendrotoxin, like Charybdotoxin, is seen to attach to the negatively-charged channel outer mouth, and a lysine residue penetrates into the selectivity filter, with the terminal amine coordinated by carbonyls, partially disrupting the outermost ion-binding site. In the remainder of the filter two densities of bound ions are observed, rather than three as observed with other toxin-blocked Kv channels. Second, a structure of Kv1.2 in Na+ solution does not show collapse or destabilization of the selectivity filter, but instead shows an intact selectivity filter with ion density in each binding site. We also attempted to image the C-type inactivated Kv1.2 W366F channel in Na+ solution, but the protein conformation was seen to be highly variable and only a low-resolution structure could be obtained. These findings present new insights into the stability of the selectivity filter and the mechanism of toxin block of this intensively studied, voltage-gated potassium channel.https://elifesciences.org/articles/89459cryoEMion selectivitydendrotoxininactivationvoltage sensorbiophysics
spellingShingle Yangyu Wu
Yangyang Yan
Youshan Yang
Shumin Bian
Alberto Rivetta
Ken Allen
Fred J Sigworth
CryoEM structures of Kv1.2 potassium channels, conducting and non-conducting
eLife
cryoEM
ion selectivity
dendrotoxin
inactivation
voltage sensor
biophysics
title CryoEM structures of Kv1.2 potassium channels, conducting and non-conducting
title_full CryoEM structures of Kv1.2 potassium channels, conducting and non-conducting
title_fullStr CryoEM structures of Kv1.2 potassium channels, conducting and non-conducting
title_full_unstemmed CryoEM structures of Kv1.2 potassium channels, conducting and non-conducting
title_short CryoEM structures of Kv1.2 potassium channels, conducting and non-conducting
title_sort cryoem structures of kv1 2 potassium channels conducting and non conducting
topic cryoEM
ion selectivity
dendrotoxin
inactivation
voltage sensor
biophysics
url https://elifesciences.org/articles/89459
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