Association and colocalization of the Kvβ1 and Kvβ2 β-subunits with Kv1 α-subunits in mammalian brain K+ channel complexes

Kenneth J. Rhodes, Brian W. Strassle, Michael M. Monaghan, Zewditu Bekele-Arcuri, Maria F. Matos, James Trimmer

Research output: Contribution to journalArticle

248 Citations (Scopus)

Abstract

The differential expression and association of cytoplasmic β-subunits with pore-forming α-subunits may contribute significantly to the complexity and heterogeneity of voltage-gated K+ channels in excitable cells. Here we examined the association and colocalization of two mammalian β-subunits, Kvβ1 and Kvβ2, with the K+ channel α-subunits Kv1.1, Kv1.2, Kv1.4, Kv1.6, and Kv2.1 in adult rat brain. Reciprocal coimmunoprecipitation experiments using subunit-specific antibodies indicated that Kvβ1 and Kvβ2 associate with all the Kv1 α-subunits examined and with each other, but not with Kv2.1. A much larger portion of the total brain pool Kv1-containing channel complexes was found associated with Kvβ2 than with Kvβ1. Single- and multiple-label immunohistochemical staining indicated that Kvβ1 codistributes extensively with Kv1.1 and Kv1.4 in cortical interneurons, in the hippocampal perforant path and mossy fiber pathways, and in the globus pallidus and substantia nigra. Kvβ2 codistributes extensively with Kv1.1 and Kv1.2 in all brain regions examined and was strikingly colocalized with these α-subunits in the juxtaparanodal region of nodes of Ranvier as well as in the axons and terminals of cerebellar basket cells. Taken together, these data provide a direct demonstration that Kvβ1 and Kvβ2 associate and colocolize with Kv1 α-subunits in native tissues and provide a biochemical and neuroanatomical basis for the differential contribution of Kv1 α- and β-subunits to electrophysiologically diverse neuronal K+ currents.

Original languageEnglish (US)
Pages (from-to)8246-8258
Number of pages13
JournalJournal of Neuroscience
Volume17
Issue number21
StatePublished - 1997
Externally publishedYes

Fingerprint

Brain
Ranvier's Nodes
Perforant Pathway
Voltage-Gated Potassium Channels
Globus Pallidus
Presynaptic Terminals
Interneurons
Substantia Nigra
Staining and Labeling
Antibodies

Keywords

  • Central nervous system
  • Cerebellum
  • Epilepsy
  • Immunoflu orescence
  • Immunohistochemistry
  • Immunoprecipitation
  • Ion channel
  • Striatum

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Rhodes, K. J., Strassle, B. W., Monaghan, M. M., Bekele-Arcuri, Z., Matos, M. F., & Trimmer, J. (1997). Association and colocalization of the Kvβ1 and Kvβ2 β-subunits with Kv1 α-subunits in mammalian brain K+ channel complexes. Journal of Neuroscience, 17(21), 8246-8258.

Association and colocalization of the Kvβ1 and Kvβ2 β-subunits with Kv1 α-subunits in mammalian brain K+ channel complexes. / Rhodes, Kenneth J.; Strassle, Brian W.; Monaghan, Michael M.; Bekele-Arcuri, Zewditu; Matos, Maria F.; Trimmer, James.

In: Journal of Neuroscience, Vol. 17, No. 21, 1997, p. 8246-8258.

Research output: Contribution to journalArticle

Rhodes, KJ, Strassle, BW, Monaghan, MM, Bekele-Arcuri, Z, Matos, MF & Trimmer, J 1997, 'Association and colocalization of the Kvβ1 and Kvβ2 β-subunits with Kv1 α-subunits in mammalian brain K+ channel complexes', Journal of Neuroscience, vol. 17, no. 21, pp. 8246-8258.
Rhodes KJ, Strassle BW, Monaghan MM, Bekele-Arcuri Z, Matos MF, Trimmer J. Association and colocalization of the Kvβ1 and Kvβ2 β-subunits with Kv1 α-subunits in mammalian brain K+ channel complexes. Journal of Neuroscience. 1997;17(21):8246-8258.
Rhodes, Kenneth J. ; Strassle, Brian W. ; Monaghan, Michael M. ; Bekele-Arcuri, Zewditu ; Matos, Maria F. ; Trimmer, James. / Association and colocalization of the Kvβ1 and Kvβ2 β-subunits with Kv1 α-subunits in mammalian brain K+ channel complexes. In: Journal of Neuroscience. 1997 ; Vol. 17, No. 21. pp. 8246-8258.
@article{0eb28b2de8324aadbaf3bb6766dd0f56,
title = "Association and colocalization of the Kvβ1 and Kvβ2 β-subunits with Kv1 α-subunits in mammalian brain K+ channel complexes",
abstract = "The differential expression and association of cytoplasmic β-subunits with pore-forming α-subunits may contribute significantly to the complexity and heterogeneity of voltage-gated K+ channels in excitable cells. Here we examined the association and colocalization of two mammalian β-subunits, Kvβ1 and Kvβ2, with the K+ channel α-subunits Kv1.1, Kv1.2, Kv1.4, Kv1.6, and Kv2.1 in adult rat brain. Reciprocal coimmunoprecipitation experiments using subunit-specific antibodies indicated that Kvβ1 and Kvβ2 associate with all the Kv1 α-subunits examined and with each other, but not with Kv2.1. A much larger portion of the total brain pool Kv1-containing channel complexes was found associated with Kvβ2 than with Kvβ1. Single- and multiple-label immunohistochemical staining indicated that Kvβ1 codistributes extensively with Kv1.1 and Kv1.4 in cortical interneurons, in the hippocampal perforant path and mossy fiber pathways, and in the globus pallidus and substantia nigra. Kvβ2 codistributes extensively with Kv1.1 and Kv1.2 in all brain regions examined and was strikingly colocalized with these α-subunits in the juxtaparanodal region of nodes of Ranvier as well as in the axons and terminals of cerebellar basket cells. Taken together, these data provide a direct demonstration that Kvβ1 and Kvβ2 associate and colocolize with Kv1 α-subunits in native tissues and provide a biochemical and neuroanatomical basis for the differential contribution of Kv1 α- and β-subunits to electrophysiologically diverse neuronal K+ currents.",
keywords = "Central nervous system, Cerebellum, Epilepsy, Immunoflu orescence, Immunohistochemistry, Immunoprecipitation, Ion channel, Striatum",
author = "Rhodes, {Kenneth J.} and Strassle, {Brian W.} and Monaghan, {Michael M.} and Zewditu Bekele-Arcuri and Matos, {Maria F.} and James Trimmer",
year = "1997",
language = "English (US)",
volume = "17",
pages = "8246--8258",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "21",

}

TY - JOUR

T1 - Association and colocalization of the Kvβ1 and Kvβ2 β-subunits with Kv1 α-subunits in mammalian brain K+ channel complexes

AU - Rhodes, Kenneth J.

AU - Strassle, Brian W.

AU - Monaghan, Michael M.

AU - Bekele-Arcuri, Zewditu

AU - Matos, Maria F.

AU - Trimmer, James

PY - 1997

Y1 - 1997

N2 - The differential expression and association of cytoplasmic β-subunits with pore-forming α-subunits may contribute significantly to the complexity and heterogeneity of voltage-gated K+ channels in excitable cells. Here we examined the association and colocalization of two mammalian β-subunits, Kvβ1 and Kvβ2, with the K+ channel α-subunits Kv1.1, Kv1.2, Kv1.4, Kv1.6, and Kv2.1 in adult rat brain. Reciprocal coimmunoprecipitation experiments using subunit-specific antibodies indicated that Kvβ1 and Kvβ2 associate with all the Kv1 α-subunits examined and with each other, but not with Kv2.1. A much larger portion of the total brain pool Kv1-containing channel complexes was found associated with Kvβ2 than with Kvβ1. Single- and multiple-label immunohistochemical staining indicated that Kvβ1 codistributes extensively with Kv1.1 and Kv1.4 in cortical interneurons, in the hippocampal perforant path and mossy fiber pathways, and in the globus pallidus and substantia nigra. Kvβ2 codistributes extensively with Kv1.1 and Kv1.2 in all brain regions examined and was strikingly colocalized with these α-subunits in the juxtaparanodal region of nodes of Ranvier as well as in the axons and terminals of cerebellar basket cells. Taken together, these data provide a direct demonstration that Kvβ1 and Kvβ2 associate and colocolize with Kv1 α-subunits in native tissues and provide a biochemical and neuroanatomical basis for the differential contribution of Kv1 α- and β-subunits to electrophysiologically diverse neuronal K+ currents.

AB - The differential expression and association of cytoplasmic β-subunits with pore-forming α-subunits may contribute significantly to the complexity and heterogeneity of voltage-gated K+ channels in excitable cells. Here we examined the association and colocalization of two mammalian β-subunits, Kvβ1 and Kvβ2, with the K+ channel α-subunits Kv1.1, Kv1.2, Kv1.4, Kv1.6, and Kv2.1 in adult rat brain. Reciprocal coimmunoprecipitation experiments using subunit-specific antibodies indicated that Kvβ1 and Kvβ2 associate with all the Kv1 α-subunits examined and with each other, but not with Kv2.1. A much larger portion of the total brain pool Kv1-containing channel complexes was found associated with Kvβ2 than with Kvβ1. Single- and multiple-label immunohistochemical staining indicated that Kvβ1 codistributes extensively with Kv1.1 and Kv1.4 in cortical interneurons, in the hippocampal perforant path and mossy fiber pathways, and in the globus pallidus and substantia nigra. Kvβ2 codistributes extensively with Kv1.1 and Kv1.2 in all brain regions examined and was strikingly colocalized with these α-subunits in the juxtaparanodal region of nodes of Ranvier as well as in the axons and terminals of cerebellar basket cells. Taken together, these data provide a direct demonstration that Kvβ1 and Kvβ2 associate and colocolize with Kv1 α-subunits in native tissues and provide a biochemical and neuroanatomical basis for the differential contribution of Kv1 α- and β-subunits to electrophysiologically diverse neuronal K+ currents.

KW - Central nervous system

KW - Cerebellum

KW - Epilepsy

KW - Immunoflu orescence

KW - Immunohistochemistry

KW - Immunoprecipitation

KW - Ion channel

KW - Striatum

UR - http://www.scopus.com/inward/record.url?scp=0030612011&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0030612011&partnerID=8YFLogxK

M3 - Article

C2 - 9334400

AN - SCOPUS:0030612011

VL - 17

SP - 8246

EP - 8258

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 21

ER -