Voltage-dependent gating of Shaker A-type potassium channels in Drosophila muscle

The voltage-dependent gating mechanism of A1-type potassium channels coded for by the Shaker locus of Drosophila was studied using macroscopic and single-channel recording techniques on embryonic myotubes in primary culture. From a kinetic analysis of data from single A1 channels, we have concluded that all of the molecular transitions after first opening, including the inactivation transition, are voltage independent and therefore not associated with charge movement through the membrane. In contrast, at least some of the activation transitions leading to first opening are considerably voltage dependent and account for all of the voltage dependence seen in the macroscopic currents. This mechanism is similar in many ways to that of vertebrate neuronal voltage-sensitive sodium channels, and together with the sequence similarities in the S4 region suggests a conserved mechanism for voltage-dependent gating among channels with different selectivities. By testing independent and coupled models for activation and inactivation we have determined that the final opening transition and inactivation are not likely to arise from the independent action of multiple subunits, each with simple gating transitions, but rather come about through their aggregate properties. A partially coupled model accurately reproduces all of the single- channel and macroscopic data. This model will provide a framework on which to organize and understand alterations in gating that occur in Shaker variants and mutants.

• Publication year

  1990

• Venue

  The Journal of General Physiology

• Publication date

  1990-01-01

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1085/JGP.95.1.29PMID 2299331PMCID 2216290
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Glial and neuronal forms of the voltage-dependent sodium channel: characteristics and cell-type distribution.

  1989cited by this paper
• Gating of single Shaker potassium channels in Drosophila muscle and in Xenopus oocytes injected with Shaker mRNA.

  1989influential reference
• Rubidium ions and the gating of delayed rectifier potassium channels of frog skeletal muscle.

  1989cited by this paper
• Kinetic properties of single sodium channels in rat heart and rat brain

  1989cited by this paper
• Expression of functional potassium channels from Shaker cDNA in Xenopus oocytes

  1988cited by this paper
• Multiple potassium-channel components are produced by alternative splicing at the shaker locus in Drosophila

  1988cited by this paper
• Restoration of excitation—contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA

  1988cited by this paper
• Four cDNA clones from the Shaker locus of Drosophila induce kinetically distinct A-type potassium currents in Xenopus oocytes.

  1988cited by this paper
• Sequence and expression of mRNAs encoding the alpha 1 and alpha 2 subunits of a DHP-sensitive calcium channel.

  1988cited by this paper
• Sequence and expression of MRNAs encoding the α1 and α2 subunits of a DHP-sensitive calcium channel

  1988cited by this paper
• Primary structure of rat brain sodium channel III deduced from the cDNA sequence

  1988cited by this paper
• Shaker encodes a family of putative potassium channel proteins in the nervous system of Drosophila.

  1988cited by this paper
• Voltage-gated potassium channels in larval CNS neurons of Drosophila

  1988cited by this paper
• Single-channel analysis of four distinct classes of potassium channels in Drosophila muscle

  1988cited by this paper
• A-type potassium channels expressed from Shaker locus cDNA.

  1988influential reference
• Multiple products of the Drosophila Shaker gene may contribute to potassium channel diversity.

  1988cited by this paper
• Charybdotoxin block of Shaker K+ channels suggests that different types of K+ channels share common structural features.

  1988cited by this paper
• Multiple potassium–channel components are produced by alternative splicing at the Shaker locus in Drosophila

  1988cited by this paper
• Selectivity and patch measurements of A‐current channels in Helix aspersa neurones.

  1987cited by this paper
• Primary structure of the receptor for calcium channel blockers from skeletal muscle

  1987cited by this paper
• Gene dosage and complementation analysis of the Shaker locus in Drosophila

  1987cited by this paper
• Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila.

  1987cited by this paper
• Molecular organization of the maternal effect region of the Shaker complex of Drosophila: characterization of an IA channel transcript with homology to vertebrate Na+ channel

  1987cited by this paper
• Voltage-dependent gating of single sodium channels from mammalian neuroblastoma cells

  1987cited by this paper
• Single-channel and genetic analyses reveal two distinct A-type potassium channels in Drosophila.

  1987cited by this paper
• Molecular characterization of Shaker, a Drosophila gene that encodes a potassium channel.

  1987cited by this paper
• Genomic organization and deduced amino acid sequence of a putative sodium channel gene in Drosophila.

  1987cited by this paper
• Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila.

  1987cited by this paper
• Existence of distinct sodium channel messenger RNAs in rat brain

  1986influential reference
• Single transient K channels in mammalian sensory neurons.

  1986cited by this paper
• Molecular model of the action potential sodium channel.

  1986cited by this paper
• Voltage-dependent gating of sodium channels: correlating structure and function

  1986cited by this paper
• Single‐channel analysis of fast transient potassium currents from rat nodose neurones.

  1985cited by this paper
• The structure of the voltage‐sensitive sodium channel

  1985cited by this paper
• Voltage clamp analysis of membrane currents in larval muscle fibers of Drosophila: alteration of potassium currents in Shaker mutants

  1985cited by this paper
• Membrane patches and whole‐cell membranes: a comparison of electrical properties in rat clonal pituitary (GH3) cells.

  1984cited by this paper
• Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence

  1984cited by this paper
• Sodium channel gating: models, mimics, and modifiers.

  1983cited by this paper
• A reinterpretation of mammalian sodium channel gating based on single channel recording

  1983cited by this paper
• Genetic and voltage-clamp analysis of a Drosophila potassium channel.

  1983cited by this paper
• Potassium currents in Drosophila: different components affected by mutations of two genes.

  1983cited by this paper
• Tight-Seal Whole-Cell Recording

  1983cited by this paper
• Sodium and calcium channels in bovine chromaffin cells

  1982cited by this paper
• Genetic modification of potassium channels in Drosophila Shaker mutants

  1981cited by this paper
• Outward currents in developing Drosophila flight muscle.

  1981cited by this paper
• Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches

  1981cited by this paper
• Preparation of cell cultures fromDrosophila melanogaster embryos

  1979cited by this paper
• Interactions between intrinsic membrane protein and electric field. An approach to studying nerve excitability.

  1978cited by this paper
• Two Mutations of synaptic transmission in Drosophila

  1977cited by this paper
• Three pharmacologically distinct potassium channels in molluscan neurones.

  1977influential reference
• Inactivation of the sodium channel. I. Sodium current experiments

  1977cited by this paper
• Inactivation of the sodium channel. II. Gating current experiments

  1977cited by this paper
• Factors affecting Drosophila neuron and myocyte differentiation in vitro

  1972cited by this paper
• Voltage clamp studies of a transient outward membrane current in gastropod neural somata

  1971cited by this paper
• Two Fast Transient Current Components during Voltage Clamp on Snail Neurons

  1971cited by this paper
• Inactivation of the Potassium Conductance and Related Phenomena Caused by Quaternary Ammonium Ion Injection in Squid Axons

  1969cited by this paper
• A quantitative description of membrane current and its application to conduction and excitation in nerve

  1952cited by this paper

• Disruption of a side portal pathway permits closed-state inactivation by BK β subunit N termini.

  2025cites this paper
• Disruption of a side portal pathway permits closed-state inactivation by BK β subunit N-termini

  2025cites this paper
• Golden Gate cloning enables efficient concatemer construction for biophysical analysis of heterozygous potassium channel variants from patients with epilepsy.

  2025cites this paper
• Subunit gating resulting from individual protonation events in Kir2 channels

  2023cites this paper
• Subunit gating resulting from individual protonation events in Kir2 channels

  2023cites this paper
• Binding of RPR260243 at the intracellular side of the hERG1 channel pore domain slows closure of the helix bundle crossing gate

  2023cites this paper
• The Evolutionary Assembly of Neuronal Machinery.

  2020cites this paper
• A perspective on Na and K channel inactivation

  2018cites this paper
• The interaction between the voltage-gated potassium channel h K v 1 . 3 and verapamil

  2018influential citation
• A Static Distributed-parameter Circuit Model Explains Electrical Stimulation on the Neuromuscular System.

  2018cites this paper
• A Structural Model of the Inactivation Gate of Voltage Activated Potassium Channels.

  2017cites this paper
• Ginsenoside Rg 3 , a Gating Modifier of EAG Family K 1 Channels s

  2016cites this paper
• Ginsenoside Rg3, a Gating Modifier of EAG Family K+ Channels

  2016cites this paper
• Voltage gating by molecular subunits of Na+ and K+ ion channels: higher-dimensional cubic kinetics, rate constants, and temperature.

  2015cites this paper
• Early-Onset Epileptic Encephalopathy Caused by Gain-of-Function Mutations in the Voltage Sensor of Kv7.2 and Kv7.3 Potassium Channel Subunits

  2015cites this paper
• Shaker IR T449 Mutants Separate C- from U-Type Inactivation

  2014cites this paper
• Chloride-driven electromechanical phase lags at acoustic frequencies are generated by SLC26a5, the outer hair cell motor protein.

  2014cites this paper
• A Conserved Pre-Block Interaction Motif Regulates Potassium Channel Activation and N-Type Inactivation

  2013cites this paper
• Structural correlates of selectivity and inactivation in potassium channels.

  2012cites this paper
• Dampening of Hyperexcitability in CA1 Pyramidal Neurons by Polyunsaturated Fatty Acids Acting on Voltage-Gated Ion Channels

  2012cites this paper
• Cardiac cell modelling: observations from the heart of the cardiac physiome project.

  2011cites this paper
• KCNE1 and KCNE2 inhibit forward trafficking of homomeric N-type voltage-gated potassium channels.

  2011cites this paper
• Couplage entre les régions IIS4-S5 et IIS6 lors de l'activation du canal calcique CaV2.3

  2011cites this paper
• An Intersubunit Interaction between S4-S5 Linker and S6 Is Responsible for the Slow Off-gating Component in Shaker K+ Channels*

  2010cites this paper
• Inactivation gating of potassium channels

  2010cites this paper
• An AUosteric Model for Calcium Channel Activation and Dihydropyrid ne Agonist Action

  2010cites this paper
• New Mechanism for Voltage Induced Charge Movement Revealed in GPCRs - Theory and Experiments

  2010cites this paper
• Crystalline, membrane-embedded, and fibrillar proteins investigated by solid-state NMR spectroscopy

  2009cites this paper
• Structural Insights into KChIP4a Modulation of Kv4.3 Inactivation*

  2009cites this paper
• Biochemistry on a leash: the roles of tether length and geometry in signal integration proteins.

  2009influential citation
• Coupling of activation and inactivation gate in a K+‐channel: potassium and ligand sensitivity

  2009cites this paper
• Disulfide locking a sodium channel voltage sensor reveals ion pair formation during activation

  2008cites this paper
• Modeling subunit cooperativity in opening of tetrameric ion channels.

  2008cites this paper
• The role of SUMO modification in the regulation of Kv1.5, a major cardiovascular potassium channel

  2008cites this paper
• Modification of K+ channel–drug interactions by ancillary subunits

  2008cites this paper
• Electrophysiological Modeling of Fibroblasts and their Interaction with Myocytes

  2007cites this paper
• Structure, function and expression of voltage-dependent sodium channels

  2007cites this paper
• A Quantitative Description of KcsA Gating I: Macroscopic Currents

  2007cites this paper
• Potassium currents in the hair cells of vestibular epithelium: position‐dependent expression of two types of A channels

  2007cites this paper
• Ion currents and spiking properties of identified subtypes of locust octopaminergic dorsal unpaired median neurons

  2006cites this paper
• A Trapped Intracellular Cation Modulates K+ Channel Recovery From Slow Inactivation

  2006influential citation
• Channel Inactivation Mechanisms

  2005cites this paper
• FPL 64176 modification of Ca(V)1.2 L-type calcium channels: dissociation of effects on ionic current and gating current.

  2005cites this paper
• Potassium channel gating in adhesion: from an oocyte–silicon to a neuron–astrocyte adhesion contact

  2005cites this paper
• Inactivation determined by a single site in K+ pores

  2004influential citation
• Molecular physiology and modulation of somatodendritic A-type potassium channels.

  2004cites this paper
• Gating Charges in the Activation and Inactivation Processes of the hERG Channel

  2004cites this paper
• Inactivation of Kv3.3 Potassium Channels in Heterologous Expression Systems*

  2003cites this paper
• Constitutive Activation of the Shaker Kv Channel

  2003cites this paper
• Calcium Channels: Unanswered Questions

  2003cites this paper
• Low Molecular Weight Poly(A) + mRNA Species Encode Factors that Modulate Gating of a non-Shaker A-Type K + Channel

  2003cites this paper
• Voltage-gated outward K currents in frog saccular hair cells.

  2003cites this paper
• pes of Inactivation in Shaker l 6 ’ Channels : Effects of Alterations in the Carboxy-Terminal Region

  2003cites this paper
• Distinctive modulatory effects of five human auxiliary beta2 subunit splice variants on L-type calcium channel gating.

  2003cites this paper
• Cholesterol modifies the gating of Kv1.3 in human T lymphocytes

  2003cites this paper
• Novel functional properties of Ca2+ channel β subunits revealed by their expression in adult rat heart cells

  2002cites this paper
• Role of Amino Acid Residues in Transmembrane Segments IS6 and IIS6 of the Na+ Channel α Subunit in Voltage-dependent Gating and Drug Block*

  2002cites this paper
• Computing Transient Gating Charge Movement of Voltage-Dependent Ion Channels

  2002cites this paper
• Computer Models of Ion Channels

  2002cites this paper
• Non-synaptic ion channels in insects--basic properties of currents and their modulation in neurons and skeletal muscles.

  2001cites this paper
• U-type inactivation of Kv3.1 and Shaker potassium channels.

  2001cites this paper
• Gating of voltage-dependent potassium channels.

  2001cites this paper
• The molecular physiology of the cardiac transient outward potassium current (I(to)) in normal and diseased myocardium.

  2001cites this paper
• Modulation of Kv1.5 potassium channel gating by extracellular zinc.

  2001cites this paper
• Potassium channel receptor site for the inactivation gate and quaternary amine inhibitors

  2001cites this paper
• Gating Properties Conferred on Bk Channels by the β3b Auxiliary Subunit in the Absence of Its Nh2- and Cooh Termini

  2001cites this paper
• Modelling of voltage-dependent gating and sodium currents in the Kv1.5 potassium channel

  2001cites this paper
• Gating charge immobilization caused by the transition between inactivated states in the Kv1.5 channel.

  2001cites this paper
• The amino side of the C‐terminus determines fast inactivation of the T‐type calcium channel α1G

  2001cites this paper
• CHAPTER 14 – Voltage-Dependent K+ Channels

  2001cites this paper
• Identification of Inactivation Determinants in the Domain IIS6 Region of High Voltage-activated Calcium Channels*

  2001cites this paper
• The voltage sensor in voltage-dependent ion channels.

  2000cites this paper
• Arachidonic acid modulation of α1H, a cloned human T-type calcium channel

  2000cites this paper
• Modulation of the Shaker K+Channel Gating Kinetics by the S3–S4 Linker

  2000cites this paper
• Cytoplasmic residues influence the voltage‐dependence of the gating of human K+ channels

  2000cites this paper
• Ionic channels in intestinal neurons

  2000cites this paper
• The kinetics of a non-inactivating K(+) current in alphaT3-1 pituitary gonadotropes is not affected by holding potential.

  2000cites this paper
• A-type potassium current in myenteric neurons from guinea-pig small intestine.

  2000cites this paper
• Arachidonic acid modulation of alpha1H, a cloned human T-type calcium channel.

  2000cites this paper
• Role of the Calcium-Independent Transient Outward Current Ito1 in Shaping Action Potential Morphology and Duration

  2000cites this paper
• A series of amino-2-cyclohexyl esters, their electrophysiological and antiarrhythmic effects as related to actions on ischemia-induced arrhythmias

  2000cites this paper
• Synthesis of the Cardiac Purkinje-fiber Action Potential Using a Computer Model

  2000cites this paper
• Voltage‐gated currents distinguish parvocellular from magnocellular neurones in the rat hypothalamic paraventricular nucleus

  2000cites this paper
• Allosteric Voltage Gating of Potassium Channels II: Mslo Channel Gating Charge Movement in the Absence of Ca2+

  1999cites this paper
• Ionic Mechanisms for the Antiarrhythmic Action of Cinnamophilin in Rat Heart

  1999cites this paper
• Human Ether-à-go-go–related Gene K+ Channel Gating Probed with Extracellular Ca2+

  1999cites this paper
• Ionic mechanisms for the antiarrhythmic action of cinnamophilin in rat heart.

  1999cites this paper
• N-type calcium channel inactivation probed by gating-current analysis.

  1999cites this paper
• Allosteric Voltage Gating of Potassium Channels I: Mslo Ionic Currents in the Absence of Ca2+

  1999cites this paper
• Molecular Dynamics of the Sodium Channel Pore Vary with Gating: Interactions between P-Segment Motions and Inactivation

  1999cites this paper
• Determinants of Voltage-Dependent Gating and Open-State Stability in the S5 Segment of Shaker Potassium Channels

  1999cites this paper
• Selective inhibition of transient K+ current by La3+ in crab peptide-secretory neurons.

  1999cites this paper
• Linear systems analysis of kinetic behaviors of calcium ion channel gating on the biological membrane by an allosteric model

  1999cites this paper
• VLG K Kv1-Shak: Vertebrate K+ channels related to Drosophila Shaker (Kvα subunits encoded by gene subfamily Kv1)

  1999cites this paper
• K+ channels lacking the 'tetramerization' domain: implications for pore structure

  1999cites this paper
• Charged drug interactions at the inner mouth of K+ channels: Information gained from gating current studies

  1999cites this paper
• Mechanism of transient outward K(+) channel block by disopyramide.

  1999cites this paper
• Potassium ion channel inactivation peptides.

  1999cites this paper
• Chapter 3 Activation of Voltage-Dependent Potassium Channels

  1999cites this paper
• H+ ion modulation of C-type inactivation of Shaker K+ channels

  1999cites this paper