Title: Remodeling neuronal ER–PM junctions is a conserved nonconducting function of Kv2 plasma membrane ion channels

Journal Article · · Molecular Biology of the Cell
 [1];  [2];  [2];  [2];  [2];  [2]
  1. Univ. of California, Davis, CA (United States); DOE/OSTI
  2. Univ. of California, Davis, CA (United States)
+ Show Author Affiliations

The endoplasmic reticulum (ER) and plasma membrane (PM) form junctions crucial to ion and lipid signaling and homeostasis. The Kv2.1 ion channel is localized at ER–PM junctions in brain neurons and is unique among PM proteins in its ability to remodel these specialized membrane contact sites. Here, we show that this function is conserved between Kv2.1 and Kv2.2, which differ in their biophysical properties, modulation, and cellular expression. Kv2.2 ER–PM junctions are present at sites deficient in the actin cytoskeleton, and disruption of the actin cytoskeleton affects their spatial organization. Kv2.2-containing ER–PM junctions overlap with those formed by canonical ER–PM tethers. The ability of Kv2 channels to remodel ER–PM junctions is unchanged by point mutations that eliminate their ion conduction but eliminated by point mutations within the Kv2-specific proximal restriction and clustering (PRC) domain that do not impact their ion channel function. The highly conserved PRC domain is sufficient to transfer the ER–PM junction–remodeling function to another PM protein. Last, brain neurons in Kv2 double-knockout mice have altered ER–PM junctions. Together, these findings demonstrate a conserved in vivo function for Kv2 family members in remodeling neuronal ER–PM junctions that is distinct from their canonical role as ion-conducting channels shaping neuronal excitability.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). The Molecular Foundry (TMF)
Sponsoring Organization:
American Heart Association (AHA); National Institutes of Health (NIH); USDOE
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1625247
Journal Information:
Molecular Biology of the Cell, Journal Name: Molecular Biology of the Cell Journal Issue: 20 Vol. 29; ISSN 1059-1524
Publisher:
American Society for Cell BiologyCopyright Statement
Country of Publication:
United States
Language:
English

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Interaction between Extracellular Hanatoxin and the Resting Conformation of the Voltage-Sensor Paddle in Kv Channels journal October 2003
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Altered Kv2.1 functioning promotes increased excitability in hippocampal neurons of an Alzheimer’s disease mouse model journal February 2016
An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways journal May 2005
Regulation of ion channel localization and phosphorylation by neuronal activity journal June 2004
Non-conducting functions of voltage-gated ion channels journal October 2006
De novo KCNB1 mutations in infantile epilepsy inhibit repetitive neuronal firing journal October 2015
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Localization-dependent activity of the Kv2.1 delayed-rectifier K+ channel journal June 2010
Phosphorylation of the voltage-gated potassium channel Kv2.1 by AMP-activated protein kinase regulates membrane excitability journal October 2011
Chemoselective tarantula toxins report voltage activation of wild-type ion channels in live cells journal October 2014
Contacts between the endoplasmic reticulum and other membranes in neurons journal May 2017
Kv2 potassium channels form endoplasmic reticulum/plasma membrane junctions via interaction with VAPA and VAPB journal June 2018
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Activity-dependent Phosphorylation of Neuronal Kv2.1 Potassium Channels by CDK5 journal June 2011
STIM1 and STIM2 Proteins Differently Regulate Endogenous Store-operated Channels in HEK293 Cells journal December 2014
Cell Cycle-dependent Changes in Localization and Phosphorylation of the Plasma Membrane Kv2.1 K + Channel Impact Endoplasmic Reticulum Membrane Contact Sites in COS-1 Cells journal October 2015
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A Gastropod Toxin Selectively Slows Early Transitions in the Shaker K Channel's Activation Pathway journal May 2004
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Cortical actin contributes to spatial organization of ER–PM junctions journal November 2017
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Kv2.1/Kv9.3, a novel ATP-dependent delayed-rectifier K+ channel in oxygen-sensitive pulmonary artery myocytes journal November 1997
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Reticulon Short Hairpin Transmembrane Domains Are Used to Shape ER Tubules journal November 2010
Focal aggregation of voltage-gated, Kv2.1 subunit-containing, potassium channels at synaptic sites in rat spinal motoneurones: Kv2.1 channel clusters in motoneurones journal February 2004
The Role of Voltage-Gated Potassium Channels Kv2.1 and Kv2.2 in the Regulation of Insulin and Somatostatin Release from Pancreatic Islets journal November 2012
Phosphorylation of the Kv2.1 K + Channel Alters Voltage-Dependent Activation journal November 1997
Graded Regulation of the Kv2.1 Potassium Channel by Variable Phosphorylation journal August 2006
Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells journal February 1983
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STIM Proteins and the Endoplasmic Reticulum-Plasma Membrane Junctions journal July 2011
Structure and Development of E-C Coupling Units in Skeletal Muscle journal October 1994
Resveratrol inhibits K v 2.2 currents through the estrogen receptor GPR30-mediated PKC pathway journal September 2013
A practical guide to evaluating colocalization in biological microscopy journal April 2011
Influence of cloned voltage-gated K+ channel expression on alanine transport, Rb+ uptake, and cell volume journal November 1993
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Roles of specific K v channel types in repolarization of the action potential in genetically identified subclasses of pyramidal neurons in mouse neocortex journal May 2016
Store-Operated Calcium Channels journal October 2015
Clinical features and outcome of 6 new patients carrying de novo KCNB1 gene mutations journal December 2017
A cytoskeletal-based perimeter fence selectively corrals a sub-population of cell surface Kv2.1 channels journal July 2007
Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains journal May 2005
Induction of stable ER-plasma-membrane junctions by Kv2.1 potassium channels journal April 2015
Developmental Expression of Kv Potassium Channels at the Axon Initial Segment of Cultured Hippocampal Neurons journal October 2012
Identification of VAPA and VAPB as Kv2 Channel-Interacting Proteins Defining Endoplasmic Reticulum–Plasma Membrane Junctions in Mammalian Brain Neurons journal July 2018
Contrasting immunohistochemical localizations in rat brain of two novel K+ channels of the Shab subfamily journal April 1993
Dynamic Regulation of the Kv2.1 Voltage-Gated Potassium Channel during Brain Ischemia through Neuroglial Interaction journal August 2008
Kv2.1 Potassium Channels Are Retained within Dynamic Cell Surface Microdomains That Are Defined by a Perimeter Fence journal September 2006
Distinct Cell- and Layer-Specific Expression Patterns and Independent Regulation of Kv2 Channel Subtypes in Cortical Pyramidal Neurons journal November 2015
Identification of the Kv2.1 K + Channel as a Major Component of the Delayed Rectifier K + Current in Rat Hippocampal Neurons journal March 1999
Delayed Rectifier K + Currents, I K , Are Encoded by Kv2 α-Subunits and Regulate Tonic Firing in Mammalian Sympathetic Neurons journal December 2002
Calcium- and Metabolic State-Dependent Modulation of the Voltage-Dependent Kv2.1 Channel Regulates Neuronal Excitability in Response to Ischemia journal November 2005
Trafficking of Kv2.1 Channels to the Axon Initial Segment by a Novel Nonconventional Secretory Pathway journal October 2017
The Kv2.1 C Terminus Can Autonomously Transfer Kv2.1-Like Phosphorylation-Dependent Localization, Voltage-Dependent Gating, and Muscarinic Modulation to Diverse Kv Channels journal January 2006
Leptin Modulates the Intrinsic Excitability of AgRP/NPY Neurons in the Arcuate Nucleus of the Hypothalamus journal April 2014
Differential Regulation of Action Potential Shape and Burst-Frequency Firing by BK and Kv2 Channels in Substantia Nigra Dopaminergic Neurons journal December 2015
Kv2.1 Clustering Contributes to Insulin Exocytosis and Rescues Human β-Cell Dysfunction journal June 2017
Blockers of the Delayed-Rectifier Potassium Current in Pancreatic  -Cells Enhance Glucose-Dependent Insulin Secretion journal March 2006
Stim and Orai proteins in neuronal Ca2+ signaling and excitability journal April 2015
Kv2 Ion Channels Determine the Expression and Localization of the Associated AMIGO-1 Cell Adhesion Molecule in Adult Brain Neurons journal January 2018
PIVlab – Towards User-friendly, Affordable and Accurate Digital Particle Image Velocimetry in MATLAB journal October 2014
Kv2.2: A Novel Molecular Target to Study the Role of Basal Forebrain GABAergic Neurons in the Sleep-Wake Cycle journal December 2013
Calcium influx through CRAC channels controls actin organization and dynamics at the immune synapse journal July 2016
GRAM domain proteins specialize functionally distinct ER-PM contact sites in human cells journal February 2018
Neurodevelopmental Disorders Caused by De Novo Variants in KCNB1 Genotypes and Phenotypes journal October 2017
De novo KCNB1 mutations in epileptic encephalopathy: KCNB1 Mutations journal September 2014
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The voltage-dependent potassium channel subunit Kv2.1 regulates insulin secretion from rodent and human islets independently of its electrical function journal March 2012
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A Novel Targeting Signal for Proximal Clustering of the Kv2.1 K+ Channel in Hippocampal Neurons journal February 2000
Interaction between Extracellular Hanatoxin and the Resting Conformation of the Voltage-Sensor Paddle in Kv Channels journal October 2003
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Kv2.1 Ablation Alters Glucose-Induced Islet Electrical Activity, Enhancing Insulin Secretion journal September 2007
STIM2 Is an Inhibitor of STIM1-Mediated Store-Operated Ca2+ Entry journal July 2006
In vitro maturation of the cisternal organelle in the hippocampal neuron's axon initial segment journal September 2011
Kv2.1: A Voltage-Gated K+ Channel Critical to Dynamic Control of Neuronal Excitability journal October 2005
Subcellular Localization of K+ Channels in Mammalian Brain Neurons: Remarkable Precision in the Midst of Extraordinary Complexity journal January 2015
Junctophilin 3 expresses in pancreatic beta cells and is required for glucose-stimulated insulin secretion journal June 2016
Altered Kv2.1 functioning promotes increased excitability in hippocampal neurons of an Alzheimer’s disease mouse model journal February 2016
An inducible translocation strategy to rapidly activate and inhibit small GTPase signaling pathways journal May 2005
Regulation of ion channel localization and phosphorylation by neuronal activity journal June 2004
Non-conducting functions of voltage-gated ion channels journal October 2006
De novo KCNB1 mutations in infantile epilepsy inhibit repetitive neuronal firing journal October 2015
The fluorescent protein palette: tools for cellular imaging journal January 2009
Identification and characterization of the STIM (stromal interaction molecule) gene family: coding for a novel class of transmembrane proteins journal July 2001
A voltage-driven switch for ion-independent signaling by ether-a-go-go K+ channels journal February 2006
E-Syts, a family of membranous Ca2+-sensor proteins with multiple C2 domains journal February 2007
Localization-dependent activity of the Kv2.1 delayed-rectifier K+ channel journal June 2010
Phosphorylation of the voltage-gated potassium channel Kv2.1 by AMP-activated protein kinase regulates membrane excitability journal October 2011
Chemoselective tarantula toxins report voltage activation of wild-type ion channels in live cells journal October 2014
Contacts between the endoplasmic reticulum and other membranes in neurons journal May 2017
Kv2 potassium channels form endoplasmic reticulum/plasma membrane junctions via interaction with VAPA and VAPB journal June 2018
Immunological identification and characterization of a delayed rectifier K+ channel polypeptide in rat brain. journal December 1991
Formation of Heteromeric Kv2 Channels in Mammalian Brain Neurons journal March 2010
Activity-dependent Phosphorylation of Neuronal Kv2.1 Potassium Channels by CDK5 journal June 2011
STIM1 and STIM2 Proteins Differently Regulate Endogenous Store-operated Channels in HEK293 Cells journal December 2014
Molecular Determinants of Kv1.3 Potassium Channels-induced Proliferation journal December 2015
Cell Cycle-dependent Changes in Localization and Phosphorylation of the Plasma Membrane Kv2.1 K + Channel Impact Endoplasmic Reticulum Membrane Contact Sites in COS-1 Cells journal October 2015
Visualization and Manipulation of Plasma Membrane-Endoplasmic Reticulum Contact Sites Indicates the Presence of Additional Molecular Components within the STIM1-Orai1 Complex journal August 2007
Nerve growth factor regulates the abundance and distribution of K+ channels in PC12 cells. journal December 1993
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Identification of a cytoplasmic domain important in the polarized expression and clustering of the Kv2.1 K+ channel. journal December 1996
Metadata matters: access to image data in the real world journal May 2010
Dynamic formation of ER–PM junctions presents a lipid phosphatase to regulate phosphoinositides journal April 2016
Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons. journal August 1976
Potassium-dependent Changes in the Conformation of the Kv2.1 Potassium Channel Pore journal June 1999
Ion–Ion Interactions at the Selectivity Filter journal April 2000
A Gastropod Toxin Selectively Slows Early Transitions in the Shaker K Channel's Activation Pathway journal May 2004
A novel epileptic encephalopathy mutation in KCNB1 disrupts Kv2.1 ion selectivity, expression, and localization journal October 2015
Single-molecule analysis of diffusion and trapping of STIM1 and Orai1 at endoplasmic reticulum–plasma membrane junctions journal November 2014
Cortical actin contributes to spatial organization of ER–PM junctions journal November 2017
Structural Plasticity of Synaptopodin in the Axon Initial Segment during Visual Cortex Development journal July 2017
Kv2.1/Kv9.3, a novel ATP-dependent delayed-rectifier K+ channel in oxygen-sensitive pulmonary artery myocytes journal November 1997
Deletion of the Kv2.1 delayed rectifier potassium channel leads to neuronal and behavioral hyperexcitability: Kv2.1 deletion and hyperexcitability journal March 2014
Frequency-dependent regulation of rat hippocampal somato-dendritic excitability by the K + channel subunit Kv2.1 journal January 2000
Reticulon Short Hairpin Transmembrane Domains Are Used to Shape ER Tubules journal November 2010
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Focal aggregation of voltage-gated, Kv2.1 subunit-containing, potassium channels at synaptic sites in rat spinal motoneurones: Kv2.1 channel clusters in motoneurones journal February 2004
Kv2 subunits underlie slowly inactivating potassium current in rat neocortical pyramidal neurons: Neocortical Kv2 channels journal June 2007
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Kv2 channels regulate firing rate in pyramidal neurons from rat sensorimotor cortex: Kv2 channels regulate firing rate in rat pyramidal neurons journal August 2013
The Role of Voltage-Gated Potassium Channels Kv2.1 and Kv2.2 in the Regulation of Insulin and Somatostatin Release from Pancreatic Islets journal November 2012
Phosphorylation of the Kv2.1 K + Channel Alters Voltage-Dependent Activation journal November 1997
Graded Regulation of the Kv2.1 Potassium Channel by Variable Phosphorylation journal August 2006
Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells journal February 1983
Endoplasmic Reticulum–Plasma Membrane Contact Sites journal June 2017
STIM Proteins and the Endoplasmic Reticulum-Plasma Membrane Junctions journal July 2011
Endoplasmic Reticulum–Plasma Membrane Associations:Structures and Functions journal October 2016
Structure and Development of E-C Coupling Units in Skeletal Muscle journal October 1994
Resveratrol inhibits K v 2.2 currents through the estrogen receptor GPR30-mediated PKC pathway journal September 2013
A practical guide to evaluating colocalization in biological microscopy journal April 2011
Influence of cloned voltage-gated K+ channel expression on alanine transport, Rb+ uptake, and cell volume journal November 1993
Roles of specific K v channel types in repolarization of the action potential in genetically identified subclasses of pyramidal neurons in mouse neocortex journal May 2016
Store-Operated Calcium Channels journal October 2015
Clinical features and outcome of 6 new patients carrying de novo KCNB1 gene mutations journal December 2017
A cytoskeletal-based perimeter fence selectively corrals a sub-population of cell surface Kv2.1 channels journal July 2007
Targeting of voltage-gated potassium channel isoforms to distinct cell surface microdomains journal May 2005
Induction of stable ER-plasma-membrane junctions by Kv2.1 potassium channels journal April 2015
Benefits and Pitfalls of Secondary Antibodies: Why Choosing the Right Secondary Is of Primary Importance journal June 2012
Developmental Expression of Kv Potassium Channels at the Axon Initial Segment of Cultured Hippocampal Neurons journal October 2012
Heterogeneity in Kv2 Channel Expression Shapes Action Potential Characteristics and Firing Patterns in CA1 versus CA2 Hippocampal Pyramidal Neurons journal July 2017
Identification of VAPA and VAPB as Kv2 Channel-Interacting Proteins Defining Endoplasmic Reticulum–Plasma Membrane Junctions in Mammalian Brain Neurons journal July 2018
Contrasting immunohistochemical localizations in rat brain of two novel K+ channels of the Shab subfamily journal April 1993
Dynamic Regulation of the Kv2.1 Voltage-Gated Potassium Channel during Brain Ischemia through Neuroglial Interaction journal August 2008
Kv2.1 Potassium Channels Are Retained within Dynamic Cell Surface Microdomains That Are Defined by a Perimeter Fence journal September 2006
Distinct Cell- and Layer-Specific Expression Patterns and Independent Regulation of Kv2 Channel Subtypes in Cortical Pyramidal Neurons journal November 2015
Identification of the Kv2.1 K + Channel as a Major Component of the Delayed Rectifier K + Current in Rat Hippocampal Neurons journal March 1999
Kv2 Channel Regulation of Action Potential Repolarization and Firing Patterns in Superior Cervical Ganglion Neurons and Hippocampal CA1 Pyramidal Neurons journal April 2014
Delayed Rectifier K + Currents, I K , Are Encoded by Kv2 α-Subunits and Regulate Tonic Firing in Mammalian Sympathetic Neurons journal December 2002
Regulation of Kv2.1 K+ Conductance by Cell Surface Channel Density journal January 2013
Calcium- and Metabolic State-Dependent Modulation of the Voltage-Dependent Kv2.1 Channel Regulates Neuronal Excitability in Response to Ischemia journal November 2005
Trafficking of Kv2.1 Channels to the Axon Initial Segment by a Novel Nonconventional Secretory Pathway journal October 2017
Bidirectional Activity-Dependent Regulation of Neuronal Ion Channel Phosphorylation journal December 2006
The Kv2.1 C Terminus Can Autonomously Transfer Kv2.1-Like Phosphorylation-Dependent Localization, Voltage-Dependent Gating, and Muscarinic Modulation to Diverse Kv Channels journal January 2006
Leptin Modulates the Intrinsic Excitability of AgRP/NPY Neurons in the Arcuate Nucleus of the Hypothalamus journal April 2014
Differential Regulation of Action Potential Shape and Burst-Frequency Firing by BK and Kv2 Channels in Substantia Nigra Dopaminergic Neurons journal December 2015
Kv2.1 Clustering Contributes to Insulin Exocytosis and Rescues Human β-Cell Dysfunction journal June 2017
Blockers of the Delayed-Rectifier Potassium Current in Pancreatic  -Cells Enhance Glucose-Dependent Insulin Secretion journal March 2006
Stim and Orai proteins in neuronal Ca2+ signaling and excitability journal April 2015
Kv2 Ion Channels Determine the Expression and Localization of the Associated AMIGO-1 Cell Adhesion Molecule in Adult Brain Neurons journal January 2018
PIVlab – Towards User-friendly, Affordable and Accurate Digital Particle Image Velocimetry in MATLAB journal October 2014
Kv2.2: A Novel Molecular Target to Study the Role of Basal Forebrain GABAergic Neurons in the Sleep-Wake Cycle journal December 2013
Calcium influx through CRAC channels controls actin organization and dynamics at the immune synapse journal July 2016
GRAM domain proteins specialize functionally distinct ER-PM contact sites in human cells journal February 2018

Cited By (11)

Kv2 channels create endoplasmic reticulum / plasma membrane junctions: a brief history of Kv2 channel subcellular localization journal January 2019
Unlocking the gating mechanism of Kv2.1 using guangxitoxin journal December 2018
Axonal Endoplasmic Reticulum Dynamics and Its Roles in Neurodegeneration. text January 2020
Sticking With It: ER-PM Membrane Contact Sites as a Coordinating Nexus for Regulating Lipids and Proteins at the Cell Cortex journal July 2020
A toolbox of nanobodies developed and validated for use as intrabodies and nanoscale immunolabels in mammalian brain neurons journal September 2019
Kv2.1 mediates spatial and functional coupling of L-type calcium channels and ryanodine receptors in mammalian neurons journal October 2019
Molecular determinants of homo- and heteromeric interactions of Junctophilin-1 at triads in adult skeletal muscle fibers journal July 2019
Kv2.1 channels play opposing roles in regulating membrane potential, Ca 2+ channel function, and myogenic tone in arterial smooth muscle journal February 2020
Neuronal ER–plasma membrane junctions organized by Kv2–VAP pairing recruit Nir proteins and affect phosphoinositide homeostasis journal October 2019
A toolbox of nanobodies developed and validated for use as intrabodies and nanoscale immunolabels in mammalian brain neurons journal September 2019
Kv2.1 mediates spatial and functional coupling of L-type calcium channels and ryanodine receptors in mammalian neurons journal October 2019

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59 BASIC BIOLOGICAL SCIENCES
Cell Biology