Molecular and cellular basis of small- and intermediate-conductance, calcium-activated potassium channel function in the brain

Abstract.Small conductance calcium-activated potassium (SK or KCa2) channels link intracellular calcium transients to membrane potential changes. SK channel subtypes present different pharmacology and distribution in the nervous system. The selective blocker apamin, SK enhancers and mice lacking specific SK channel subunits have revealed multifaceted functions of these channels in neurons, glia and cerebral blood vessels. SK channels regulate neuronal firing by contributing to the afterhyperpolarization following action potentials and mediating IAHP, and partake in a calcium-mediated feedback loop with NMDA receptors, controlling the threshold for induction of hippocampal long-term potentiation. The function of distinct SK channel subtypes in different neurons often results from their specific coupling to different calcium sources. The prominent role of SK channels in the modulation of excitability and synaptic function of limbic, dopaminergic and cerebellar neurons hints at their possible involvement in neuronal dysfunction, either as part of the causal mechanism or as potential therapeutic targets.

[1]  J. Furness,et al.  The distribution of intermediate‐conductance, calcium‐activated, potassium (IK) channels in epithelial cells , 2006, Journal of anatomy.

[2]  D. Strøbæk,et al.  Selective positive modulation of the SK3 and SK2 subtypes of small conductance Ca2+‐activated K+ channels , 2007, British journal of pharmacology.

[3]  Charles J. Wilson,et al.  Apamin-Sensitive Small Conductance Calcium-Activated Potassium Channels, through their Selective Coupling to Voltage-Gated Calcium Channels, Are Critical Determinants of the Precision, Pace, and Pattern of Action Potential Generation in Rat Subthalamic Nucleus Neurons In Vitro , 2003, The Journal of Neuroscience.

[4]  P. Schwindt,et al.  Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. , 1988, Journal of neurophysiology.

[5]  M. Alda,et al.  Lack of association between the hSKCa3 channel gene CAG polymorphism and schizophrenia. , 1999, American journal of medical genetics.

[6]  V. Kaushal,et al.  The Ca2+-Activated K+ Channel KCNN4/KCa3.1 Contributes to Microglia Activation and Nitric Oxide-Dependent Neurodegeneration , 2007, The Journal of Neuroscience.

[7]  H. Rochat,et al.  Characterization of a new leiurotoxin I‐like scorpion toxin , 1993, FEBS letters.

[8]  E. Galván,et al.  Calcium-activated afterhyperpolarizations regulate synchronization and timing of epileptiform bursts in hippocampal CA3 pyramidal neurons. , 2006, Journal of neurophysiology.

[9]  A. Weston,et al.  Endothelium-derived hyperpolarizing factor: a new endogenous inhibitor from the vascular endothelium. , 1988, Trends in pharmacological sciences.

[10]  K. Chandy,et al.  Design and Characterization of a Highly Selective Peptide Inhibitor of the Small Conductance Calcium-activated K+Channel, SkCa2* , 2001, The Journal of Biological Chemistry.

[11]  Abraham Weizman,et al.  CAG repeat polymorphism within the KCNN3 gene is a significant contributor to susceptibility to anorexia nervosa: A case‐control study of female patients and several ethnic groups in the Israeli Jewish population , 2004, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[12]  D. Strøbæk,et al.  Pharmacological characterization of small‐conductance Ca2+‐activated K+ channels stably expressed in HEK 293 cells , 2000, British journal of pharmacology.

[13]  Philip M. Groves,et al.  Statistical properties of neuronal spike trains in the substantia nigra: Cell types and their interactions , 1977, Brain Research.

[14]  H. Ujike,et al.  Association study of CAG repeats in the KCNN3 gene in Japanese patients with schizophrenia, schizoaffective disorder and bipolar disorder , 2001, Psychiatry Research.

[15]  T. Begenisich,et al.  Physiological Roles of the Intermediate Conductance, Ca2+-activated Potassium Channel Kcnn4* , 2004, Journal of Biological Chemistry.

[16]  Y. Nakane,et al.  Lack of association between the hKCa3 gene and Japanese schizophrenia patients , 2001, Psychiatric genetics.

[17]  P. Vanhoutte,et al.  Characterization of an apamin‐sensitive small‐conductance Ca2+‐activated K+ channel in porcine coronary artery endothelium: relevance to EDHF , 2002, British journal of pharmacology.

[18]  C. Lupica,et al.  Independent Presynaptic and Postsynaptic Mechanisms Regulate Endocannabinoid Signaling at Multiple Synapses in the Ventral Tegmental Area , 2004, The Journal of Neuroscience.

[19]  Abraham Weizman,et al.  An association of CAG repeats at the KCNN3 locus with symptom dimensions of schizophrenia , 2002, Biological Psychiatry.

[20]  R. Margolis,et al.  Family-based association analysis of the hSKCa3 potassium channel gene in bipolar disorder , 1999, Molecular Psychiatry.

[21]  F. Faraci,et al.  Responses of cerebral arterioles to ADP: eNOS-dependent and eNOS-independent mechanisms. , 2004, American journal of physiology. Heart and circulatory physiology.

[22]  T. Svensson.  Dysfunctional brain dopamine systems induced by psychotomimetic NMDA-receptor antagonists and the effects of antipsychotic drugs , 2000, Brain Research Reviews.

[23]  Lucien T. Thompson,et al.  Apamin increases excitability of CA1 hippocampal pyramidal neurons , 2000 .

[24]  A. Marty,et al.  Ca-dependent K channels with large unitary conductance in chromaffin cell membranes , 1981, Nature.

[25]  Rodrigo Andrade,et al.  SKCa Channels Mediate the Medium But Not the Slow Calcium-Activated Afterhyperpolarization in Cortical Neurons , 2004, The Journal of Neuroscience.

[26]  J. Scuvée-Moreau,et al.  Modulation of small conductance calcium-activated potassium (SK) channels: a new challenge in medicinal chemistry. , 2003, Current medicinal chemistry.

[27]  J. Adelman,et al.  Regulation of Surface Localization of the Small Conductance Ca2+-activated Potassium Channel, Sk2, through Direct Phosphorylation by cAMP-dependent Protein Kinase* , 2006, Journal of Biological Chemistry.

[28]  K. Hsiao,et al.  Genetic association study of a polymorphic CAG repeats array of calcium-activated potassium channel (KCNN3) gene and schizophrenia among the Chinese population from Taiwan , 1999, Molecular Psychiatry.

[29]  H. Rochat,et al.  Chemical synthesis and structure-activity relationships of Ts kappa, a novel scorpion toxin acting on apamin-sensitive SK channel. , 1999, The journal of peptide research : official journal of the American Peptide Society.

[30]  B. Bunney,et al.  Firing properties of substantia nigra dopaminergic neurons in freely moving rats. , 1985, Life sciences.

[31]  Contextual memory deficits observed in mice overexpressing small conductance Ca 2+ -activated , 2008 .

[32]  K. Reymann,et al.  Inhibition of apamin-sensitive calcium dependent potassium channels facilitate the induction of long-term potentiation in the CA1 region of rat hippocampus in vitro , 1998, Neuroscience Letters.

[33]  R. Roth,et al.  Extracellular dopamine and neurotensin in rat prefrontal cortex in vivo: effects of median forebrain bundle stimulation frequency, stimulation pattern, and dopamine autoreceptors , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  O. McManus,et al.  High-conductance calcium-activated potassium channels; Structure, pharmacology, and function , 1996, Journal of bioenergetics and biomembranes.

[35]  R. Lea,et al.  Association analysis of a highly polymorphic CAG Repeat in the human potassium channel gene KCNN3 and migraine susceptibility , 2005, BMC Medical Genetics.

[36]  M. Rietschel,et al.  hSKCa3: no association of the polymorphic CAG repeat with bipolar affective disorder and schizophrenia. , 1999, Psychiatric genetics.

[37]  Scott M Thompson,et al.  Unique roles of SK and Kv4.2 potassium channels in dendritic integration. , 2004, Neuron.

[38]  D. G. Haylett,et al.  K+ currents generated by NMDA receptor activation in rat hippocampal pyramidal neurons. , 2002, Journal of neurophysiology.

[39]  Anders Björklund,et al.  Prospects for new restorative and neuroprotective treatments in Parkinson's disease , 1999, Nature.

[40]  D. Strøbæk,et al.  Specific Enhancement of SK Channel Activity Selectively Potentiates the Afterhyperpolarizing Current IAHP and Modulates the Firing Properties of Hippocampal Pyramidal Neurons* , 2005, Journal of Biological Chemistry.

[41]  V. Gross,et al.  Impaired Endothelium-Derived Hyperpolarizing Factor–Mediated Dilations and Increased Blood Pressure in Mice Deficient of the Intermediate-Conductance Ca2+-Activated K+ Channel , 2006, Circulation research.

[42]  M. Koronyo-Hamaoui,et al.  Association study of CAG repeats in the KCNN3 gene in Israeli patients with major psychosis , 2003, Psychiatric genetics.

[43]  S. Grissmer,et al.  K+ channel types targeted by synthetic OSK1, a toxin from Orthochirus scrobiculosus scorpion venom. , 2005, The Biochemical journal.

[44]  D. Linden,et al.  Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. , 1999, Journal of neurophysiology.

[45]  M. Mann,et al.  Protein Kinase CK2 Is Coassembled with Small Conductance Ca2+-Activated K+ Channels and Regulates Channel Gating , 2004, Neuron.

[46]  K. Chandy,et al.  Design of a potent and selective inhibitor of the intermediate-conductance Ca2+-activated K+ channel, IKCa1: a potential immunosuppressant. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[47]  P. Sah,et al.  Channels underlying neuronal calcium-activated potassium currents , 2002, Progress in Neurobiology.

[48]  A. Damjanović,et al.  SCHIZOPHRENIA AND POLYMORPHIC CAG REPEATS ARRAY OF CALCIUM-ACTIVATED POTASSIUM CHANNEL (KCNN3) GENE IN SERBIAN POPULATION , 2006, The International journal of neuroscience.

[49]  John Gordon Ralph Jefferys,et al.  Ca2+ entry through l-type Ca2+ channels helps terminate epileptiform activity by activation of a Ca2+ dependent afterhyperpolarisation in hippocampal CA3. , 2001, Neuroscience.

[50]  G. Giménez-Gallego,et al.  Purification and characterization of a unique, potent inhibitor of apamin binding from Leiurus quinquestriatus hebraeus venom. , 1988, The Journal of biological chemistry.

[51]  H Rauer,et al.  Structural Conservation of the Pores of Calcium-activated and Voltage-gated Potassium Channels Determined by a Sea Anemone Toxin* , 1999, The Journal of Biological Chemistry.

[52]  S. Grissmer,et al.  The human Ca2+-activated K+ channel, IK, can be blocked by the tricyclic antihistamine promethazine , 2006, Neuropharmacology.

[53]  S. T. Kitai,et al.  Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra , 1993, Neuroscience Research.

[54]  M. Cheeran,et al.  Role of Microglia in Central Nervous System Infections , 2004, Clinical Microbiology Reviews.

[55]  N. Mercuri,et al.  Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  K. Chandy,et al.  Delineation of the Clotrimazole/TRAM-34 Binding Site on the Intermediate Conductance Calcium-activated Potassium Channel, IKCa1* , 2001, The Journal of Biological Chemistry.

[57]  Hua Hu,et al.  Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after‐hyperpolarization and excitability control in CA1 hippocampal pyramidal cells , 2005, The Journal of physiology.

[58]  D. G. Haylett,et al.  Enhancement of Hippocampal Pyramidal Cell Excitability by the Novel Selective Slow-Afterhyperpolarization Channel Blocker 3-(Triphenylmethylaminomethyl)pyridine (UCL2077) , 2006, Molecular Pharmacology.

[59]  H. Jahnsen,et al.  Electrophysiological characteristics of neurones in the guinea‐pig deep cerebellar nuclei in vitro. , 1986, The Journal of physiology.

[60]  Kamran Khodakhah,et al.  Somatic and Dendritic Small-Conductance Calcium-Activated Potassium Channels Regulate the Output of Cerebellar Purkinje Neurons , 2003, The Journal of Neuroscience.

[61]  J. Storm,et al.  Regional Differences in Distribution and Functional Expression of Small-Conductance Ca2+-Activated K+ Channels in Rat Brain , 2002, The Journal of Neuroscience.

[62]  A. K. Singh,et al.  Modulation of Cl- secretion by benzimidazolones. I. Direct activation of a Ca(2+)-dependent K+ channel. , 1996, The American journal of physiology.

[63]  D. G. Haylett,et al.  The SK3 Subunit of Small Conductance Ca2+-activated K+ Channels Interacts with Both SK1 and SK2 Subunits in a Heterologous Expression System* , 2004, Journal of Biological Chemistry.

[64]  S. Sandow,et al.  Evidence for Involvement of Both IKCa and SKCa Channels in Hyperpolarizing Responses of the Rat Middle Cerebral Artery , 2006, Stroke.

[65]  Pharmacological characterisation of the human small conductance calcium-activated potassium channel hSK3 reveals sensitivity to tricyclic antidepressants and antipsychotic phenothiazines , 2001, Neuropharmacology.

[66]  M. Eckmann,et al.  Role of endothelial intermediate conductance KCa channels in cerebral EDHF-mediated dilations. , 2003, American journal of physiology. Heart and circulatory physiology.

[67]  M. T. Roberts,et al.  Block of rat brain recombinant SK channels by tricyclic antidepressants and related compounds. , 2000, European journal of pharmacology.

[68]  S. Tate,et al.  The distribution of small and intermediate conductance calcium-activated potassium channels in the rat sensory nervous system , 2005, Neuroscience.

[69]  R. S. Waters,et al.  Specificity in the interaction of HVA Ca2+ channel types with Ca2+-dependent AHPs and firing behavior in neocortical pyramidal neurons. , 1998, Journal of neurophysiology.

[70]  F. Edwards,et al.  The ducky2J Mutation in Cacna2d2 Results in Reduced Spontaneous Purkinje Cell Activity and Altered Gene Expression , 2006, The Journal of Neuroscience.

[71]  J. Furness,et al.  Intermediate‐conductance calcium‐activated potassium channels in enteric neurones of the mouse: pharmacological, molecular and immunochemical evidence for their role in mediating the slow afterhyperpolarization , 2004, Journal of neurochemistry.

[72]  R. Latorre,et al.  New disguises for an old channel: MaxiK channel beta-subunits. , 2002, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[73]  I. Gottesman,et al.  Lack of association between schizophrenia and a CAG repeat polymorphism of the hSKCa3 gene in a North Eastern US sample , 2000, Molecular Psychiatry.

[74]  Dominique Debanne,et al.  Long-Term Enhancement of Neuronal Excitability and Temporal Fidelity Mediated by Metabotropic Glutamate Receptor Subtype 5 , 2003, The Journal of Neuroscience.

[75]  H. Kimelberg,et al.  Serotonin induces inward potassium and calcium currents in rat cortical astrocytes , 1997, Brain Research.

[76]  T. Ishii,et al.  A human intermediate conductance calcium-activated potassium channel. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[77]  Ping Hx,et al.  Apamin-sensitive Ca2+-activated K+ channels regulate pacemaker activity in nigral dopamine neurons , 1996 .

[78]  Thanos Tzounopoulos,et al.  Small Conductance Ca2+-Activated K+Channels Modulate Synaptic Plasticity and Memory Encoding , 2002, The Journal of Neuroscience.

[79]  W. Schultz.  Multiple reward signals in the brain , 2000, Nature Reviews Neuroscience.

[80]  J. Furness,et al.  Intermediate conductance potassium (IK) channels occur in human enteric neurons , 2004, Autonomic Neuroscience.

[81]  C. Austin,et al.  Mapping of hKCa3 to chromosome 1q21 and investigation of linkage of CAG repeat polymorphism to schizophrenia , 1999, Molecular Psychiatry.

[82]  Charles J. Wilson,et al.  Origin of the slow afterhyperpolarization and slow rhythmic bursting in striatal cholinergic interneurons. , 2006, Journal of neurophysiology.

[83]  P. Vanhoutte,et al.  Characterization of a charybdotoxin‐sensitive intermediate conductance Ca2+‐activated K+ channel in porcine coronary endothelium: relevance to EDHF , 2002, British journal of pharmacology.

[84]  P. Seeburg,et al.  Respiration and parturition affected by conditional overexpression of the Ca2+-activated K+ channel subunit, SK3. , 2000, Science.

[85]  A. Bruening-Wright,et al.  Bicuculline block of small-conductance calcium-activated potassium channels , 1999, Pflügers Archiv.

[86]  S. Olesen,et al.  Apamin interacts with all subtypes of cloned small-conductance Ca2+-activated K+ channels , 2000, Pflügers Archiv.

[87]  J. J. Couey,et al.  Modulation of recombinant and native neuronal SK channels by the neuroprotective drug riluzole. , 2002, European journal of pharmacology.

[88]  B. Sabatini,et al.  Nonlinear Regulation of Unitary Synaptic Signals by CaV2.3 Voltage-Sensitive Calcium Channels Located in Dendritic Spines , 2007, Neuron.

[89]  D. Trezise,et al.  Partial apamin sensitivity of human small conductance Ca2+-activated K+ channels stably expressed in Chinese hamster ovary cells , 2002, Naunyn-Schmiedeberg's Archives of Pharmacology.

[90]  Xiaoping Xu,et al.  Large-conductance, calcium-activated potassium channels: structural and functional implications. , 2006, Pharmacology & therapeutics.

[91]  K. Chandy,et al.  Calmodulin Mediates Calcium-dependent Activation of the Intermediate Conductance KCa Channel,IKCa1 * , 1999, The Journal of Biological Chemistry.

[92]  A. Dresse,et al.  Calcium release from internal stores is required for the generation of spontaneous hyperpolarizations in dopaminergic neurons of neonatal rats. , 2000, Journal of neurophysiology.

[93]  P. Shepard,et al.  SK Ca2+-activated K+ channel ligands alter the firing pattern of dopamine-containing neurons in vivo , 2006, Neuroscience.

[94]  G. Kirov,et al.  No evidence of association from transmission disequilibrium analysis of the hKCa3 gene in bipolar disorder. , 2000, Bipolar disorders.

[95]  W. Bunney,et al.  Novel truncated isoform of SK3 potassium channel is a potent dominant-negative regulator of SK currents: implications in schizophrenia , 2003, Molecular Psychiatry.

[96]  U. Misgeld,et al.  Ca2+ release‐dependent hyperpolarizations modulate the firing pattern of juvenile GABA neurons in mouse substantia nigra pars reticulata in vitro , 2006, The Journal of physiology.

[97]  D. Pietrobon.  Function and dysfunction of synaptic calcium channels: insights from mouse models , 2005, Current Opinion in Neurobiology.

[98]  Anthony A Grace,et al.  Gating of information flow within the limbic system and the pathophysiology of schizophrenia , 2000, Brain Research Reviews.

[99]  A. Verkhratsky,et al.  Glial calcium: homeostasis and signaling function. , 1998, Physiological reviews.

[100]  Pankaj Sah,et al.  Physiological Role of Calcium-Activated Potassium Currents in the Rat Lateral Amygdala , 2002, The Journal of Neuroscience.

[101]  E. Hirsch,et al.  Rescue of Mesencephalic Dopaminergic Neurons in Culture by Low-Level Stimulation of Voltage-Gated Sodium Channels , 2004, The Journal of Neuroscience.

[102]  R. Stackman,et al.  Small-Conductance Ca 2-Activated K Channel Type 2 ( SK 2 ) Modulates Hippocampal Learning , Memory , and Synaptic Plasticity , 2006 .

[103]  P. Pedarzani,et al.  Domain Analysis of the Calcium-activated Potassium Channel SK1 from Rat Brain , 2004, Journal of Biological Chemistry.

[104]  E. Blanc,et al.  Solution structure of TsKapa, a charybdotoxin‐like scorpion toxin from Tityus serrulatus with high affinity for apamin‐sensitive Ca2+‐activated K+ channels , 1997, Proteins.

[105]  V. Calderone.  Large-conductance, ca(2+)-activated k(+) channels: function, pharmacology and drugs. , 2002, Current medicinal chemistry.

[106]  S Fletcher,et al.  Somatic Colocalization of Rat SK1 and D class (Cav 1.2) L-type Calcium Channels in Rat CA1 Hippocampal Pyramidal Neurons , 2001, The Journal of Neuroscience.

[107]  T. Strassmaier,et al.  A Novel Isoform of SK2 Assembles with Other SK Subunits in Mouse Brain* , 2005, Journal of Biological Chemistry.

[108]  R. Rimini,et al.  Quantitative expression analysis of the small conductance calcium-activated potassium channels, SK1, SK2 and SK3, in human brain. , 2000, Brain research. Molecular brain research.

[109]  R. Latorre,et al.  New Disguises for an Old Channel: MaxiK Channel β-Subunits , 2002 .

[110]  J. Adelman,et al.  Regional distribution of SK3 mRNA‐containing neurons in the adult and adolescent rat ventral midbrain and their relationship to dopamine‐containing cells , 2004, Synapse.

[111]  G. Gutman,et al.  A piece in the puzzle: an ion channel candidate gene for schizophrenia. , 1998, Molecular medicine today.

[112]  M. Womack,et al.  Dendritic Control of Spontaneous Bursting in Cerebellar Purkinje Cells , 2004, The Journal of Neuroscience.

[113]  M. Martina,et al.  The sigma‐1 receptor modulates NMDA receptor synaptic transmission and plasticity via SK channels in rat hippocampus , 2007, The Journal of physiology.

[114]  D. Geschwind,et al.  Association of moderate polyglutamine tract expansions in the slow calcium-activated potassium channel type 3 with ataxia. , 2001, Archives of neurology.

[115]  A. Grace.  Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: A hypothesis for the etiology of schizophrenia , 1991, Neuroscience.

[116]  O. Riess,et al.  Length variation of a polyglutamine array in the gene encoding a small-conductance, calcium-activated potassium channel (hKCa3) and susceptibility to idiopathic generalized epilepsy , 1999, Epilepsy Research.

[117]  M. Womack,et al.  Calcium-Activated Potassium Channels Are Selectively Coupled to P/Q-Type Calcium Channels in Cerebellar Purkinje Neurons , 2004, The Journal of Neuroscience.

[118]  Egidio D'Angelo,et al.  Ionic mechanisms of autorhythmic firing in rat cerebellar Golgi cells , 2006, The Journal of physiology.

[119]  P. Pedarzani,et al.  An apamin-sensitive Ca2+-activated K+ current in hippocampal pyramidal neurons. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[120]  M. Shah,et al.  The pharmacology of hSK1 Ca2+‐activated K+ channels expressed in mammalian cell lines , 2000, British journal of pharmacology.

[121]  T. Otis,et al.  Blessed are the pacemakers , 2006, Nature Neuroscience.

[122]  D. G. Haylett,et al.  Small Conductance Ca2+‐Activated K+ Channels Formed by the Expression of Rat SK1 and SK2 Genes in HEK 293 Cells , 2003, The Journal of physiology.

[123]  J. Kao,et al.  Hyperexcitability of Distal Dendrites in Hippocampal Pyramidal Cells after Chronic Partial Deafferentation , 2007, The Journal of Neuroscience.

[124]  H. Repp,et al.  Lysophospholipids induce membrane hyperpolarization in microglia by activation of IKCa1 Ca2+-dependent K+ channels , 2002, Neuroscience.

[125]  N. Marrion,et al.  Gating of Recombinant Small-Conductance Ca-activated K+ Channels by Calcium , 1998, The Journal of general physiology.

[126]  A. Bruening-Wright,et al.  Structure and complex transcription pattern of the mouse SK1 K(Ca) channel gene, KCNN1. , 2001, Biochimica et biophysica acta.

[127]  L. Salkoff,et al.  High-conductance potassium channels of the SLO family , 2006, Nature Reviews Neuroscience.

[128]  B. Fakler,et al.  Organization and Regulation of Small Conductance Ca2+-activated K+ Channel Multiprotein Complexes , 2007, The Journal of Neuroscience.

[129]  Kamran Khodakhah,et al.  Decreases in the precision of Purkinje cell pacemaking cause cerebellar dysfunction and ataxia , 2006, Nature Neuroscience.

[130]  P. Pedarzani,et al.  Medium afterhyperpolarization and firing pattern modulation in interneurons of stratum radiatum in the CA3 hippocampal region. , 2001, Journal of neurophysiology.

[131]  N. Craddock,et al.  Further support for an association between a polymorphic CAG repeat in the hKCa3 gene and schizophrenia , 1998, Molecular Psychiatry.

[132]  Jochen Roeper,et al.  Selective Coupling of T-Type Calcium Channels to SK Potassium Channels Prevents Intrinsic Bursting in Dopaminergic Midbrain Neurons , 2002, The Journal of Neuroscience.

[133]  B. Lancaster,et al.  SK channels and the varieties of slow after‐hyperpolarizations in neurons , 2003, The European journal of neuroscience.

[134]  S. G. Taylor,et al.  Endothelium-derived hyperpolarizing a new endogenous inhibitor from the vascular endothelium , 1988 .

[135]  H. Wulff,et al.  Modulators of small- and intermediate-conductance calcium-activated potassium channels and their therapeutic indications. , 2007, Current medicinal chemistry.

[136]  J. Adelman,et al.  SK channels in excitability, pacemaking and synaptic integration , 2005, Current Opinion in Neurobiology.

[137]  P. Pedarzani,et al.  Differential Distribution of Three Ca2+-Activated K+ Channel Subunits, SK1, SK2, and SK3, in the Adult Rat Central Nervous System , 2000, Molecular and Cellular Neuroscience.

[138]  Activation of SK channels inhibits epileptiform bursting in hippocampal CA3 neurons , 2005, Brain Research.

[139]  S. Faraone,et al.  CAG‐Repeat length in exon 1 of KCNN3 does not influence risk for schizophrenia or bipolar disorder: A meta‐analysis of association studies , 2003, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[140]  P. Sham,et al.  Association and linkage studies between bipolar affective disorder and the polymorphic CAG/CTG repeat loci ERDA1, SEF2-1B, MAB21L and KCNN3 , 2001, Molecular Psychiatry.

[141]  Charles J. Wilson,et al.  Intrinsic Membrane Properties Underlying Spontaneous Tonic Firing in Neostriatal Cholinergic Interneurons , 2000, The Journal of Neuroscience.

[142]  A. Schwab,et al.  Functional importance of Ca2+‐activated K+ channels for lysophosphatidic acid‐induced microglial migration , 2004, The European journal of neuroscience.

[143]  M. Lazdunski,et al.  Leiurotoxin I (scyllatoxin), a peptide ligand for Ca2(+)-activated K+ channels. Chemical synthesis, radiolabeling, and receptor characterization. , 1990, The Journal of biological chemistry.

[144]  J. Stocker,et al.  Maurotoxin: a potent inhibitor of intermediate conductance Ca2+-activated potassium channels. , 2003, Molecular pharmacology.

[145]  R. Foehring,et al.  Relationship between repetitive firing and afterhyperpolarizations in human neocortical neurons. , 1992, Journal of neurophysiology.

[146]  B. Sabatini,et al.  SK channels and NMDA receptors form a Ca2+-mediated feedback loop in dendritic spines , 2005, Nature Neuroscience.

[147]  D. Strøbæk,et al.  Inhibitory Gating Modulation of Small Conductance Ca2+-Activated K+ Channels by the Synthetic Compound (R)-N-(Benzimidazol-2-yl)-1,2,3,4-tetrahydro-1-naphtylamine (NS8593) Reduces Afterhyperpolarizing Current in Hippocampal CA1 Neurons , 2006, Molecular Pharmacology.

[148]  R. Stackman,et al.  Contextual memory deficits observed in mice overexpressing small conductance Ca2+-activated K+ type 2 (KCa2.2, SK2) channels are caused by an encoding deficit. , 2008, Learning & memory.

[149]  Kamran Khodakhah,et al.  Selective regulation of spontaneous activity of neurons of the deep cerebellar nuclei by N‐type calcium channels in juvenile rats , 2008, The Journal of physiology.

[150]  P. Thier,et al.  Two types of neurons in the rat cerebellar nuclei as distinguished by membrane potentials and intracellular fillings. , 2001, Journal of neurophysiology.

[151]  S. Slough,et al.  In vivo characterisation of the small-conductance KCa (SK) channel activator 1-ethyl-2-benzimidazolinone (1-EBIO) as a potential anticonvulsant. , 2006, European journal of pharmacology.

[152]  D. Jenkinson,et al.  SK3 is an important component of K+ channels mediating the afterhyperpolarization in cultured rat SCG neurones , 2001, The Journal of physiology.

[153]  E. Carlier,et al.  Chemical synthesis and characterization of Pi1, a scorpion toxin from Pandinus imperator active on K+ channels. , 2000, European journal of biochemistry.

[154]  J. Adelman,et al.  Immunocytochemical localization of small‐conductance, calcium‐dependent potassium channels in astrocytes of the rat supraoptic nucleus , 2005, The Journal of comparative neurology.

[155]  A. Grace,et al.  Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission , 2003, Nature Neuroscience.

[156]  F. Weiss,et al.  The dopamine hypothesis of reward: past and current status , 1999, Trends in Neurosciences.

[157]  P. Shepard,et al.  Afferent modulation of dopamine neuron firing patterns , 1999, Current Opinion in Neurobiology.

[158]  D. German,et al.  Subtypes of substantia nigra dopaminergic neurons revealed by apamin: Autoradiographic and electrophysiological studies , 1992, Brain Research Bulletin.

[159]  A. Dickenson,et al.  A Functional Role for Small-Conductance Calcium-Activated Potassium Channels in Sensory Pathways Including Nociceptive Processes , 2005, The Journal of Neuroscience.

[160]  M. Rietschel,et al.  Association between hSKCa3 and schizophrenia not confirmed by transmission disequilibrium test in 193 offspring/parents trios , 1999, Molecular Psychiatry.

[161]  P. Anand,et al.  Calcium-activated potassium channel SK1- and IK1-like immunoreactivity in injured human sensory neurones and its regulation by neurotrophic factors. , 2002, Brain : a journal of neurology.

[162]  L. Jones,et al.  Mutation screening of the KCNN3 gene reveals a rare frameshift mutation , 2001, Molecular Psychiatry.

[163]  M. Lynch,et al.  Long-term potentiation and memory. , 2004, Physiological reviews.

[164]  J. Adelman,et al.  Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin , 2001, Nature.

[165]  R. Busse,et al.  EDHF: bringing the concepts together. , 2002, Trends in pharmacological sciences.

[166]  G. Lynch,et al.  A Novel Mechanism for the Facilitation of Theta-Induced Long-Term Potentiation by Brain-Derived Neurotrophic Factor , 2004, The Journal of Neuroscience.

[167]  K. Magleby,et al.  Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture , 1981, Nature.

[168]  H. Bergman,et al.  The primate subthalamic nucleus. I. Functional properties in intact animals. , 1994, Journal of neurophysiology.

[169]  Nelson Spruston,et al.  Stability and plasticity of intrinsic membrane properties in hippocampal CA1 pyramidal neurons: effects of internal anions , 2007, The Journal of physiology.

[170]  L. Kaczmarek,et al.  hSK4, a member of a novel subfamily of calcium-activated potassium channels. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[171]  A. Grace,et al.  The control of firing pattern in nigral dopamine neurons: single spike firing , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[172]  Mark S Taylor,et al.  Altered Expression of Small‐Conductance Ca2+‐Activated K+ (SK3) Channels Modulates Arterial Tone and Blood Pressure , 2003, Circulation research.

[173]  N. Marrion,et al.  Small-Conductance, Calcium-Activated Potassium Channels from Mammalian Brain , 1996, Science.

[174]  H. Rochat,et al.  Characterization of PO1, a new peptide ligand of the apamin-sensitive Ca2+ activated K+ channel. , 2009, International journal of peptide and protein research.

[175]  M. Stocker.  Ca2+-activated K+ channels: molecular determinants and function of the SK family , 2004, Nature Reviews Neuroscience.

[176]  Charles J. Wilson,et al.  Control of Spontaneous Firing Patterns by the Selective Coupling of Calcium Currents to Calcium-Activated Potassium Currents in Striatal Cholinergic Interneurons , 2005, The Journal of Neuroscience.

[177]  A. Grace,et al.  Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[178]  Mark J. Miller,et al.  Nuclear Localization and Dominant-negative Suppression by a Mutant SKCa3 N-terminal Channel Fragment Identified in a Patient with Schizophrenia* , 2001, The Journal of Biological Chemistry.

[179]  R. Emsley,et al.  CAG repeat polymorphisms in KCNN3 (HSKCa3) and PPP2R2B show no association or linkage to schizophrenia , 2003, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[180]  A. Silahtaroglu,et al.  Characterization of the cloned human intermediate-conductance Ca2+-activated K+ channel. , 1998, American journal of physiology. Cell physiology.

[181]  X. Zhu,et al.  K+ channels and the microglial respiratory burst. , 2001, American journal of physiology. Cell physiology.

[182]  J. Power,et al.  The amygdaloid complex: anatomy and physiology. , 2003, Physiological reviews.

[183]  G. Gallo,et al.  Transient PKA Activity Is Required for Initiation But Not Maintenance of BDNF-Mediated Protection from Nitric Oxide-Induced Growth-Cone Collapse , 2002, The Journal of Neuroscience.

[184]  K. Lesch,et al.  Short CAG repeats within the hSKCa3 gene associated with schizophrenia: results of a family‐based study , 1998, Neuroreport.

[185]  R. Latorre,et al.  Large conductance Ca2+-activated K+ (BK) channel: activation by Ca2+ and voltage. , 2006, Biological research.

[186]  R. Murray,et al.  Transmission disequilibrium analysis of a triplet repeat within the hKCa3 gene using family trios with schizophrenia. , 1998, Biochemical and biophysical research communications.

[187]  Johan F. Storm,et al.  Kv 7 / KCNQ / M and HCN / h , but not KCa 2 / SK channels , contribute to the somatic medium after-hyperpolarization and excitability control in CA 1 hippocampal pyramidal cells , 2005 .

[188]  S. Grissmer,et al.  An apamin- and scyllatoxin-insensitive isoform of the human SK3 channel. , 2004, Molecular pharmacology.

[189]  K. Chandy,et al.  Enhanced neuronal excitability in the absence of neurodegeneration induces cerebellar ataxia. , 2004, The Journal of clinical investigation.

[190]  G A Gutman,et al.  Isolation of a novel potassium channel gene hSKCa3 containing a polymorphic CAG repeat: a candidate for schizophrenia and bipolar disorder? , 1998, Molecular Psychiatry.

[191]  Block of maurotoxin and charybdotoxin on human intermediate-conductance calcium-activated potassium channels (hIKCa1). , 2004, Toxicon : official journal of the International Society on Toxinology.

[192]  U. Misgeld,et al.  Two pathways for the activation of small-conductance potassium channels in neurons of substantia nigra pars reticulata , 2005, Neuroscience.

[193]  Mark J. Miller,et al.  Selective blockers and manipulated channel expression levels , 2001 .

[194]  P. Goldman-Rakic,et al.  The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia , 1999, Biological Psychiatry.

[195]  D. Strøbæk,et al.  Activation of the human intermediate-conductance Ca(2+)-activated K(+) channel by 1-ethyl-2-benzimidazolinone is strongly Ca(2+)-dependent. , 1999, Biochimica et biophysica acta.

[196]  T. Teyler.  Long-term potentiation and memory. , 1987, International journal of neurology.

[197]  Jean-François Liégeois,et al.  SK channels control the firing pattern of midbrain dopaminergic neurons in vivo , 2005, The European journal of neuroscience.

[198]  Jiwon Kim,et al.  CAG repeats of CTG18.1 and KCNN3 in Korean patients with bipolar affective disorder. , 2001, Journal of affective disorders.

[199]  Kamilla Angelo,et al.  Pharmacological modulation of SK3 channels , 2001, Neuropharmacology.

[200]  Mark J. Miller,et al.  Calcium-activated Potassium Channels Sustain Calcium Signaling in T Lymphocytes , 2001, The Journal of Biological Chemistry.

[201]  M. Sanghera,et al.  Electrophysiological properties of mouse dopamine neurons: In vivo and in vitro studies , 1984, Neuroscience.

[202]  Steven W. Johnson,et al.  Bicuculline methiodide potentiates NMDA-dependent burst firing in rat dopamine neurons by blocking apamin-sensitive Ca2+-activated K+ currents , 1997, Neuroscience Letters.

[203]  P. Overton,et al.  Burst firing in midbrain dopaminergic neurons , 1997, Brain Research Reviews.

[204]  H X Ping,et al.  Apamin‐sensitive Ca2+-activated K+ channels regulate pacemaker activity in nigral dopamine neurons , 1996, Neuroreport.

[205]  P. Pedarzani,et al.  Matching molecules to function: neuronal Ca2+-activated K+ channels and afterhyperpolarizations. , 2004, Toxicon : official journal of the International Society on Toxinology.

[206]  G. Terstappen,et al.  The antidepressant fluoxetine blocks the human small conductance calcium-activated potassium channels SK1, SK2 and SK3 , 2003, Neuroscience Letters.

[207]  F. Gonon,et al.  Regulation of dopamine release by impulse flow and by autoreceptors as studied by in vivo voltammetry in the rat striatum , 1985, Neuroscience.

[208]  A. Jauch,et al.  The human small conductance calcium-regulated potassium channel gene (hSKCa3) contains two CAG repeats in exon 1, is on chromosome 1q21.3, and shows a possible association with schizophrenia , 1998, Neurogenetics.

[209]  A. K. Singh,et al.  Benzimidazolone activators of chloride secretion: potential therapeutics for cystic fibrosis and chronic obstructive pulmonary disease. , 2001, The Journal of pharmacology and experimental therapeutics.

[210]  P. Majumder,et al.  Association analysis of CAG repeats at the KCNN3 locus in Indian patients with bipolar disorder and schizophrenia. , 2000, American journal of medical genetics.

[211]  Abraham Weizman,et al.  Dual contribution of NR2B subunit of NMDA receptor and SK3 Ca(2+)-activated K+ channel to genetic predisposition to anorexia nervosa. , 2007, Journal of psychiatric research.

[212]  A. Janowsky,et al.  Domains Responsible for Constitutive and Ca2+-Dependent Interactions between Calmodulin and Small Conductance Ca2+-Activated Potassium Channels , 1999, The Journal of Neuroscience.

[213]  M. Gill,et al.  No evidence to support the association of the potassium channel gene hSKCa3 CAG repeat with schizophrenia or bipolar disorder in the Irish population , 1999, Molecular Psychiatry.

[214]  R. Stackman,et al.  Small Conductance Ca2+-Activated K+ Channel Knock-Out Mice Reveal the Identity of Calcium-Dependent Afterhyperpolarization Currents , 2004, The Journal of Neuroscience.

[215]  R. Latorre,et al.  Large conductance Ca 2 +-activated K + ( BK ) channel : Activation by Ca 2 + and voltage , 2006 .

[216]  J. Furness,et al.  Expression of intermediate conductance potassium channel immunoreactivity in neurons and epithelial cells of the rat gastrointestinal tract , 2003, Cell and Tissue Research.

[217]  E. Christian,et al.  A Novel Gene, hKCa4, Encodes the Calcium-activated Potassium Channel in Human T Lymphocytes* , 1997, The Journal of Biological Chemistry.

[218]  E. Galván,et al.  1-Ethyl-2-benzimidazolinone (EBIO) suppresses epileptiform activity in in vitro hippocampus , 2005, Neuropharmacology.

[219]  G. Edwards,et al.  Potassium and potassium clouds in endothelium-dependent hyperpolarizations. , 2004, Pharmacological research.

[220]  J. Mallet,et al.  No evidence for involvement of KCNN3 (hSKCa3) potassium channel gene in familial and isolated cases of schizophrenia , 1999, European Journal of Human Genetics.

[221]  B. Bunney,et al.  Effects of apamin on the discharge properties of putative dopamine-containing neurons in vitro , 1988, Brain Research.

[222]  J. Scuvée-Moreau,et al.  Electrophysiological characterization of the SK channel blockers methyl‐laudanosine and methyl‐noscapine in cell lines and rat brain slices , 2004, British journal of pharmacology.

[223]  V. Bolanos-Garcia,et al.  Protein kinase CK2 as an ectokinase: The role of the regulatory CK2β subunit , 2008, Proceedings of the National Academy of Sciences.

[224]  Jochen Roeper,et al.  Differential Expression of the Small-Conductance, Calcium-Activated Potassium Channel SK3 Is Critical for Pacemaker Control in Dopaminergic Midbrain Neurons , 2001, The Journal of Neuroscience.

[225]  Abraham Weizman,et al.  Association between anorexia nervosa and the hsKCa3 gene: a family-based and case control study , 2002, Molecular Psychiatry.

[226]  B. Bunney,et al.  Repetitive firing properties of putative dopamine-containing neurons in vitro: regulation by an apamin-sensitive Ca2+-activated K+ conductance , 2004, Experimental Brain Research.

[227]  J. Dostrovsky,et al.  High-frequency Synchronization of Neuronal Activity in the Subthalamic Nucleus of Parkinsonian Patients with Limb Tremor , 2000, The Journal of Neuroscience.

[228]  M. T. Roberts,et al.  Modulation of recombinant small-conductance Ca(2+)-activated K(+) channels by the muscle relaxant chlorzoxazone and structurally related compounds. , 2001, The Journal of pharmacology and experimental therapeutics.

[229]  R. Weizman,et al.  hKCa3/KCNN3 potassium channel gene: association of longer CAG repeats with schizophrenia in Israeli Ashkenazi Jews, expression in human tissues and localization to chromosome 1q21 , 1999, Molecular Psychiatry.

[230]  Nobuo Kato,et al.  Small-conductance Ca2+-dependent K+ channels are the target of spike-induced Ca2+ release in a feedback regulation of pyramidal cell excitability. , 2004, Journal of neurophysiology.

[231]  David L Downie,et al.  Novel 384-Well Population Patch Clamp Electrophysiology Assays for Ca2+-Activated K+ Channels , 2007, Journal of biomolecular screening.

[232]  P. Schwindt,et al.  Calcium-dependent potassium currents in neurons from cat sensorimotor cortex. , 1992, Journal of neurophysiology.

[233]  Masahiko Watanabe,et al.  SK2 channel plasticity contributes to LTP at Schaffer collateral–CA1 synapses , 2008, Nature Neuroscience.

[234]  A. Grace,et al.  The control of firing pattern in nigral dopamine neurons: burst firing , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[235]  Mark J. Miller,et al.  Up-regulation of the IKCa1 Potassium Channel during T-cell Activation , 2000, The Journal of Biological Chemistry.

[236]  P. Bougis,et al.  Characterization of a new peptide from Tityus serrulatus scorpion venom which is a ligand of the apamin‐binding site , 1996, FEBS letters.

[237]  Steven W. Johnson,et al.  Apamin increases NMDA-induced burst-firing of rat mesencephalic dopamine neurons , 1993, Brain Research.

[238]  B. Fakler,et al.  Control of Electrical Activity in Central Neurons by Modulating the Gating of Small Conductance Ca2+-activated K+ Channels* , 2001, The Journal of Biological Chemistry.

[239]  M. Kye,et al.  Small-conductance, Ca2+-activated K+ channel SK3 generates age-related memory and LTP deficits , 2003, Nature Neuroscience.

[240]  D. Housman,et al.  Lack of linkage or association between schizophrenia and the polymorphic trinucleotide repeat within the KCNN3 gene on chromosome 1q21. , 1999, American journal of medical genetics.

[241]  T. Ishii,et al.  Determinants of Apamin and d-Tubocurarine Block in SK Potassium Channels* , 1997, The Journal of Biological Chemistry.

[242]  Teresa Ferraro,et al.  An Amino Acid Outside the Pore Region Influences Apamin Sensitivity in Small Conductance Ca2+-activated K+ Channels* , 2006, Journal of Biological Chemistry.

[243]  J. Edgerton,et al.  Distinct contributions of small and large conductance Ca2+‐activated K+ channels to rat Purkinje neuron function , 2003, The Journal of physiology.

[244]  S. Grissmer,et al.  Characterization of the outer pore region of the apamin-sensitive Ca2+-activated K+ channel rSK2. , 2004, Toxicon : official journal of the International Society on Toxinology.

[245]  V. Bolanos-Garcia,et al.  Protein kinase CK 2 as an ectokinase : The role of the regulatory CK 2 subunit , 2008 .

[246]  T. Kita,et al.  Electrical membrane properties of rat substantia nigra compacta neurons in an in vitro slice preparation , 1986, Brain Research.

[247]  W. Honer,et al.  Location of a major susceptibility locus for familial schizophrenia on chromosome 1q21-q22. , 2000, Science.

[248]  P. Pedarzani,et al.  Developmental Regulation of Small-Conductance Ca2+-Activated K+ Channel Expression and Function in Rat Purkinje Neurons , 2002, The Journal of Neuroscience.

[249]  G. Obermair,et al.  The small conductance Ca2+‐activated K+ channel SK3 is localized in nerve terminals of excitatory synapses of cultured mouse hippocampal neurons , 2003, The European journal of neuroscience.

[250]  Nigel Emptage,et al.  Ca2+ and synaptic plasticity. , 2005, Cell calcium.

[251]  P. Sah,et al.  SK channels regulate excitatory synaptic transmission and plasticity in the lateral amygdala , 2005, Nature Neuroscience.

[252]  N. Craddock,et al.  No association between a polymorphic CAG repeat in the human potassium channel gene hKCa3 and bipolar disorder. , 1999, American journal of medical genetics.

[253]  C. Freitag,et al.  A Highly Polymorphic Poly‐Glutamine Stretch in the Potassium Channel KCNN3 in Migraine , 2005, Headache.

[254]  T. Takeuchi,et al.  Expression of the small conductance Ca2+-activated K+ channel, SK3, in the olfactory ensheathing glial cells of rat brain , 2003, Cell and Tissue Research.

[255]  Sequential and opposite regulation of two outward K(+) currents by ET-1 in cultured striatal astrocytes. , 2001, American journal of physiology. Cell physiology.

[256]  G. Terstappen,et al.  Distribution of the messenger RNA for the small conductance calcium-activated potassium channel SK3 in the adult rat brain and correlation with immunoreactivity , 2001, Neuroscience.

[257]  A. K. Singh,et al.  Pharmacological activation of cloned intermediate- and small-conductance Ca(2+)-activated K(+) channels. , 2000, American journal of physiology. Cell physiology.

[258]  B. S. Rothberg.  Allosteric Modulation of Ion Channels: The Case of Maxi-K , 2004, Science's STKE.

[259]  Yasuo Kawaguchi,et al.  Heterogeneity of phasic cholinergic signaling in neocortical neurons. , 2007, Journal of neurophysiology.

[260]  P. Christophersen,et al.  Activation of human IK and SK Ca2+ -activated K+ channels by NS309 (6,7-dichloro-1H-indole-2,3-dione 3-oxime). , 2004, Biochimica et biophysica acta.

[261]  C. Garland,et al.  Possible Role for K+ in Endothelium-Derived Hyperpolarizing Factor–Linked Dilatation in Rat Middle Cerebral Artery , 2005, Stroke.

[262]  F. Faraci,et al.  Endothelium-Derived Hyperpolarizing Factor: Where Are We Now? , 2006, Arteriosclerosis, thrombosis, and vascular biology.

[263]  J. Marksteiner,et al.  Comparative immunohistochemical distribution of three small-conductance Ca2+-activated potassium channel subunits, SK1, SK2, and SK3 in mouse brain , 2004, Molecular and Cellular Neuroscience.

[264]  J. Wickens,et al.  Modulation of an Afterhyperpolarization by the Substantia Nigra Induces Pauses in the Tonic Firing of Striatal Cholinergic Interneurons , 2004, The Journal of Neuroscience.

[265]  H. Rochat,et al.  Chemical synthesis and characterization of maurotoxin, a short scorpion toxin with four disulfide bridges that acts on K+ channels. , 1996, European journal of biochemistry.

[266]  Matthew A. Fury,et al.  Molecular BKology: The Study of Splicing and Dicing , 2002, Science's STKE.

[267]  R. Stackman,et al.  Small-Conductance Ca2+-Activated K+ Channel Type 2 (SK2) Modulates Hippocampal Learning, Memory, and Synaptic Plasticity , 2006, The Journal of Neuroscience.

[268]  J. Scuvée-Moreau,et al.  Spontaneous apamin-sensitive hyperpolarizations in dopaminergic neurons of neonatal rats. , 1998, Journal of neurophysiology.

[269]  G. Terstappen,et al.  Presynaptic localization of the small conductance calcium-activated potassium channel SK3 at the neuromuscular junction , 2001, Neuroscience.

[270]  J. Joseph,et al.  Tamapin, a Venom Peptide from the Indian Red Scorpion (Mesobuthus tamulus) That Targets Small Conductance Ca2+-activated K+ Channels and Afterhyperpolarization Currents in Central Neurons* , 2002, The Journal of Biological Chemistry.

[271]  山田 伸一郎.  Small conductance Ca[2+]-dependent K[+] channels are the target of spike-induced Ca[2+] release in a feedback regulation of pyramidal cell excitability , 2004 .

[272]  P. Strong,et al.  Identification of two toxins from scorpion (Leiurus quinquestriatus) venom which block distinct classes of calcium‐activated potassium channel , 1986, FEBS letters.

[273]  T. Ishii,et al.  Mechanism of calcium gating in small-conductance calcium-activated potassium channels , 1998, Nature.