Home LiteratureArticle Details
PMID: 15356203 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

KChIPs and Kv4 alpha subunits as integral components of A-type potassium channels in mammalian brain.

Rhodes KJ, Carroll KI, Sung MA, Doliveira LC, Monaghan MM, Burke SL, Strassle BW, Buchwalder L, Menegola M, Cao J, An WF, Trimmer JS

Abstract

Voltage-gated potassium (Kv) channels from the Kv4, or Shal-related, gene family underlie a major component of the A-type potassium current in mammalian central neurons. We recently identified a family of calcium-binding proteins, termed KChIPs (Kv channel interacting proteins), that bind to the cytoplasmic N termini of Kv4 family alpha subunits and modulate their surface density, inactivation kinetics, and rate of recovery from inactivation (An et al., 2000). Here, we used single and double-label immunohistochemistry, together with circumscribed lesions and coimmunoprecipitation analyses, to examine the regional and subcellular distribution of KChIPs1-4 and Kv4 family alpha subunits in adult rat brain. Immunohistochemical staining using KChIP-specific monoclonal antibodies revealed that the KChIP polypeptides are concentrated in neuronal somata and dendrites where their cellular and subcellular distribution overlaps, in an isoform-specific manner, with that of Kv4.2 and Kv4.3. For example, immunoreactivity for KChIP1 and Kv4.3 is concentrated in the somata and dendrites of hippocampal, striatal, and neocortical interneurons. Immunoreactivity for KChIP2, KChIP4, and Kv4.2 is concentrated in the apical and basal dendrites of hippocampal and neocortical pyramidal cells. Double-label immunofluorescence labeling revealed that throughout the forebrain, KChIP2 and KChIP4 are frequently colocalized with Kv4.2, whereas in cortical, hippocampal, and striatal interneurons, KChIP1 is frequently colocalized with Kv4.3. Coimmunoprecipitation analyses confirmed that all KChIPs coassociate with Kv4 alpha subunits in brain membranes, indicating that KChIPs 1-4 are integral components of native A-type Kv channel complexes and are likely to play a major role as modulators of somatodendritic excitability.

MeSH Terms
Animals Antibodies, Monoclonal/immunology Antibody Specificity Brain Chemistry COS Cells Calcium-Binding Proteins/physiology Chlorocebus aethiops Corpus Striatum/cytology,metabolism Dendrites/chemistry,ultrastructure Hippocampus/cytology,drug effects,metabolism Ibotenic Acid/toxicity Immunoprecipitation Interneurons/chemistry,physiology Kv Channel-Interacting Proteins Mice Mice, Inbred BALB C Microscopy, Fluorescence Neocortex/cytology,metabolism Neuronal Plasticity Neurons/chemistry,drug effects,physiology Potassium Channels/physiology Potassium Channels, Voltage-Gated/physiology Protein Interaction Mapping Protein Subunits Rats Recombinant Fusion Proteins/physiology Repressor Proteins/physiology Shal Potassium Channels Synaptic Transmission/physiology Transfection
Chemicals
Antibodies, Monoclonal Calcium-Binding Proteins Csen protein, mouse Kcnd2 protein, rat Kcnd3 protein, mouse Kcnd3 protein, rat Kcnip1 protein, mouse Kcnip1 protein, rat Kcnip2 protein, mouse Kcnip2 protein, rat Kcnip3 protein, rat Kcnip4 protein, rat Kv Channel-Interacting Proteins Potassium Channels Potassium Channels, Voltage-Gated Protein Subunits Recombinant Fusion Proteins Repressor Proteins Shal Potassium Channels Ibotenic Acid
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Rhodes Kenneth J
Neuroscience, Wyeth Discovery Research, Princeton, New Jersey 08543, USA.
Carroll Karen I
Sung M Amy
Doliveira Lisa C
Monaghan Michael M
Burke Sharon L
Strassle Brian W
Buchwalder Lynn
Menegola Milena
Cao Jie
An W Frank
Trimmer James S
References (63)
63 references, click to expand
  1. DREAM is a Ca2+-regulated transcriptional repressor.
    Nature. 1999 Mar 4;398(6722):80-4 PMID: 10078534
  2. Dendritic calcium spike initiation and repolarization are controlled by distinct potassium channel subtypes in CA1 pyramidal neurons.
    J Neurosci. 1999 Oct 15;19(20):8789-98 PMID: 10516298
  3. Kv4.2 mRNA abundance and A-type K(+) current amplitude are linearly related in basal ganglia and basal forebrain neurons.
    J Neurosci. 2000 Jan 15;20(2):579-88 PMID: 10632587
  4. Modulation of A-type potassium channels by a family of calcium sensors.
    Nature. 2000 Feb 3;403(6769):553-6 PMID: 10676964
  5. Dendritic potassium channels in hippocampal pyramidal neurons.
    J Physiol. 2000 May 15;525 Pt 1:75-81 PMID: 10811726
  6. K(+) channels and their distribution in large cortical pyramidal neurones.
    J Physiol. 2000 Jun 15;525 Pt 3:565-6 PMID: 10856111
  7. Properties of voltage-gated potassium currents in nucleated patches from large layer 5 cortical pyramidal neurons of the rat.
    J Physiol. 2000 Jun 15;525 Pt 3:593-609 PMID: 10856115
  8. Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large layer 5 cortical pyramidal neurons of the rat.
    J Physiol. 2000 Jun 15;525 Pt 3:611-20 PMID: 10856116
  9. Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients.
    J Physiol. 2000 Jun 15;525 Pt 3:621-39 PMID: 10856117
  10. Input-specific immunolocalization of differentially phosphorylated Kv4.2 in the mouse brain.
    Learn Mem. 2000 Sep-Oct;7(5):321-32 PMID: 11040264
  11. Conserved Kv4 N-terminal domain critical for effects of Kv channel-interacting protein 2.2 on channel expression and gating.
    J Biol Chem. 2001 Jun 29;276(26):23888-94 PMID: 11287421
  12. Kinetic modulation of Kv4-mediated A-current by arachidonic acid is dependent on potassium channel interacting proteins.
    J Neurosci. 2001 Jun 15;21(12):4154-61 PMID: 11404400
  13. Experimental localization of Kv1 family voltage-gated K+ channel alpha and beta subunits in rat hippocampal formation.
    J Neurosci. 2001 Aug 15;21(16):5973-83 PMID: 11487620
  14. Tuning pacemaker frequency of individual dopaminergic neurons by Kv4.3L and KChip3.1 transcription.
    EMBO J. 2001 Oct 15;20(20):5715-24 PMID: 11598014
  15. hKChIP2 is a functional modifier of hKv4.3 potassium channels: cloning and expression of a short hKChIP2 splice variant.
    Cardiovasc Res. 2001 Nov;52(2):255-64 PMID: 11684073
  16. Subcellular localization of presenilin 2 endoproteolytic C-terminal fragments.
    Brain Res Mol Brain Res. 2001 Nov 30;96(1-2):14-20 PMID: 11731004
  17. Evidence for the presence of a novel Kv4-mediated A-type K(+) channel-modifying factor.
    J Physiol. 2001 Dec 15;537(Pt 3):801-9 PMID: 11744756
  18. Gating, modulation and subunit composition of voltage-gated K(+) channels in dendritic inhibitory interneurones of rat hippocampus.
    J Physiol. 2002 Jan 15;538(Pt 2):405-19 PMID: 11790809
  19. DREAM is a critical transcriptional repressor for pain modulation.
    Cell. 2002 Jan 11;108(1):31-43 PMID: 11792319
  20. Elimination of fast inactivation in Kv4 A-type potassium channels by an auxiliary subunit domain.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):1035-40 PMID: 11805342
  21. Molecular cloning and characterization of CALP/KChIP4, a novel EF-hand protein interacting with presenilin 2 and voltage-gated potassium channel subunit Kv4.
    J Biol Chem. 2002 Apr 26;277(17):14965-75 PMID: 11847232
  22. Heterogeneous expression of KChIP2 isoforms in the ferret heart.
    J Physiol. 2002 Mar 15;539(Pt 3):649-56 PMID: 11897837
  23. Role of heteromultimers in the generation of myocardial transient outward K+ currents.
    Circ Res. 2002 Mar 22;90(5):586-93 PMID: 11909823
  24. Biochemical and immunocytochemical characterization of calsenilin in mouse brain.
    Neuroscience. 2002;114(1):247-63 PMID: 12207970
  25. PKA modulation of Kv4.2-encoded A-type potassium channels requires formation of a supramolecular complex.
    J Neurosci. 2002 Dec 1;22(23):10123-33 PMID: 12451113
  26. The CD26-related dipeptidyl aminopeptidase-like protein DPPX is a critical component of neuronal A-type K+ channels.
    Neuron. 2003 Feb 6;37(3):449-61 PMID: 12575952
  27. Functional properties of a brain-specific NH2-terminally spliced modulator of Kv4 channels.
    Am J Physiol Cell Physiol. 2003 Jul;285(1):C161-70 PMID: 12646414
  28. Active dendrites, potassium channels and synaptic plasticity.
    Philos Trans R Soc Lond B Biol Sci. 2003 Apr 29;358(1432):667-74 PMID: 12740112
  29. A fundamental role for KChIPs in determining the molecular properties and trafficking of Kv4.2 potassium channels.
    J Biol Chem. 2003 Sep 19;278(38):36445-54 PMID: 12829703
  30. Ito channels are octomeric complexes with four subunits of each Kv4.2 and K+ channel-interacting protein 2.
    J Biol Chem. 2004 Feb 13;279(7):5549-54 PMID: 14623880
  31. International Union of Pharmacology. XLI. Compendium of voltage-gated ion channels: potassium channels.
    Pharmacol Rev. 2003 Dec;55(4):583-6 PMID: 14657415
  32. Regulation of Kv4.3 voltage-dependent gating kinetics by KChIP2 isoforms.
    J Physiol. 2004 May 15;557(Pt 1):19-41 PMID: 14724186
  33. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites.
    Nat Neurosci. 2004 Feb;7(2):126-35 PMID: 14730307
  34. Localization of voltage-gated ion channels in mammalian brain.
    Annu Rev Physiol. 2004;66:477-519 PMID: 14977411
  35. Subcellular segregation of two A-type K+ channel proteins in rat central neurons.
    Neuron. 1992 Aug;9(2):271-84 PMID: 1497894
  36. Three-dimensional structure of I(to); Kv4.2-KChIP2 ion channels by electron microscopy at 21 Angstrom resolution.
    Neuron. 2004 Feb 19;41(4):513-9 PMID: 14980201
  37. Structural insights into the functional interaction of KChIP1 with Shal-type K(+) channels.
    Neuron. 2004 Feb 19;41(4):573-86 PMID: 14980206
  38. Two N-terminal domains of Kv4 K(+) channels regulate binding to and modulation by KChIP1.
    Neuron. 2004 Feb 19;41(4):587-98 PMID: 14980207
  39. Novel KChIP2 isoforms increase functional diversity of transient outward potassium currents.
    J Physiol. 2004 Jun 15;557(Pt 3):761-72 PMID: 15107477
  40. Two pharmacologically and kinetically distinct transient potassium currents in cultured embryonic mouse hippocampal neurons.
    J Neurosci. 1992 Jun;12(6):2235-46 PMID: 1607938
  41. Characterization of a mammalian cDNA for an inactivating voltage-sensitive K+ channel.
    Neuron. 1991 Sep;7(3):471-83 PMID: 1840649
  42. Immunological identification and characterization of a delayed rectifier K+ channel polypeptide in rat brain.
    Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10764-8 PMID: 1961744
  43. Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure.
    J Histochem Cytochem. 1986 Nov;34(11):1431-8 PMID: 2430009
  44. Monoclonal antibody to a membrane glycoprotein inhibits the acrosome reaction and associated Ca2+ and H+ fluxes of sea urchin sperm.
    Cell. 1985 Mar;40(3):697-703 PMID: 2982502
  45. At least two mRNA species contribute to the properties of rat brain A-type potassium channels expressed in Xenopus oocytes.
    Neuron. 1988 Oct;1(8):649-58 PMID: 3272183
  46. Association and colocalization of K+ channel alpha- and beta-subunit polypeptides in rat brain.
    J Neurosci. 1995 Jul;15(7 Pt 2):5360-71 PMID: 7623158
  47. Differential spatiotemporal expression of K+ channel polypeptides in rat hippocampal neurons developing in situ and in vitro.
    J Neurosci. 1995 May;15(5 Pt 2):3840-51 PMID: 7751950
  48. Identification of molecular components of A-type channels activating at subthreshold potentials.
    J Neurophysiol. 1994 Oct;72(4):1516-29 PMID: 7823083
  49. Low molecular weight poly(A)+ mRNA species encode factors that modulate gating of a non-Shaker A-type K+ channel.
    J Gen Physiol. 1993 Oct;102(4):713-28 PMID: 7903683
  50. Presynaptic A-current based on heteromultimeric K+ channels detected in vivo.
    Nature. 1993 Sep 2;365(6441):72-5 PMID: 8361540
  51. Cloning of a novel component of A-type K+ channels operating at subthreshold potentials with unique expression in heart and brain.
    J Neurophysiol. 1996 May;75(5):2174-9 PMID: 8734615
  52. Voltage-gated K+ channel beta subunits: expression and distribution of Kv beta 1 and Kv beta 2 in adult rat brain.
    J Neurosci. 1996 Aug 15;16(16):4846-60 PMID: 8756417
  53. Generation and characterization of subtype-specific monoclonal antibodies to K+ channel alpha- and beta-subunit polypeptides.
    Neuropharmacology. 1996;35(7):851-65 PMID: 8938716
  54. Identification of a cytoplasmic domain important in the polarized expression and clustering of the Kv2.1 K+ channel.
    J Cell Biol. 1996 Dec;135(6 Pt 1):1619-32 PMID: 8978827
  55. Cloning, expression and CNS distribution of Kv4.3, an A-type K+ channel alpha subunit.
    FEBS Lett. 1997 Jan 3;400(2):215-20 PMID: 9001401
  56. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons.
    Nature. 1997 Jun 26;387(6636):869-75 PMID: 9202119
  57. Association and colocalization of the Kvbeta1 and Kvbeta2 beta-subunits with Kv1 alpha-subunits in mammalian brain K+ channel complexes.
    J Neurosci. 1997 Nov 1;17(21):8246-58 PMID: 9334400
  58. Modulation of Kv4 channels, key components of rat ventricular transient outward K+ current, by PKC.
    Am J Physiol. 1997 Oct;273(4):H1775-86 PMID: 9362243
  59. Differential expression of Kv4 K+ channel subunits mediating subthreshold transient K+ (A-type) currents in rat brain.
    J Neurophysiol. 1998 Feb;79(2):1081-91 PMID: 9463463
  60. The K+ channel, Kv2.1, is apposed to astrocytic processes and is associated with inhibitory postsynaptic membranes in hippocampal and cortical principal neurons and inhibitory interneurons.
    Neuroscience. 1998 May;84(1):37-48 PMID: 9522360
  61. Somatodendritic depolarization-activated potassium currents in rat neostriatal cholinergic interneurons are predominantly of the A type and attributable to coexpression of Kv4.2 and Kv4.1 subunits.
    J Neurosci. 1998 May 1;18(9):3124-37 PMID: 9547221
  62. Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC.
    J Neurosci. 1998 May 15;18(10):3521-8 PMID: 9570783
  63. Calsenilin: a calcium-binding protein that interacts with the presenilins and regulates the levels of a presenilin fragment.
    Nat Med. 1998 Oct;4(10):1177-81 PMID: 9771752
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2004-09-08
Pages
7903-15
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6729940
Subset
IM
Grants
NINDS NIH HHS · R01 NS042225 · United States
NINDS NIH HHS · NS42225 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]