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PMID: 16513667 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Effects of divalent cations and spermine on the K+ channel TASK-3 and on the outward current in thalamic neurons.

The Journal of physiology ·Vol. 572 ·No. Pt 3 ·2006-05-01 ·Pages 639-57

Musset B, Meuth SG, Liu GX, Derst C, Wegner S, Pape HC, Budde T, Preisig-Müller R, Daut J

Abstract

The potassium channels TASK-1 and TASK-3 show high sequence homology but differ in their sensitivity to extracellular divalent cations. Heterologous expression in HEK293 cells showed that the single-channel conductance of TASK-3 increased approximately four-fold after removal of external divalent cations, whereas the conductance of TASK-1 was unaffected. Replacing the glutamate at position 70 of TASK-3 by a lysine or arginine residue abolished the sensitivity to divalent cations. The reverse mutation in TASK-1 (K70E) induced sensitivity to divalent cations. The organic polycations spermine and ruthenium red modulated the conductance of TASK-3 in a similar way as Ca2+ or Mg2+. Our data suggest that these effects were mediated by shielding of the negative charges in the extracellular loops of TASK-3. Whole-cell currents carried by TASK-3 channels were inhibited by spermine and ruthenium red even in the presence of external divalent cations. These data suggest that, in addition to their effect on single-channel conductance, spermine and ruthenium red decreased the open probability of TASK-3 channels, probably by binding to residue E70. The standing outward current in thalamocortical relay neurons, which is largely carried by TASK channels, was also inhibited by divalent cations and spermine. Using the differential sensitivity of TASK-1 and TASK-3 to divalent cations and spermine we found that about 20% of the standing outward current in thalamocortical relay neurons flows through TASK-3 channels. We conclude from our results that inhibition of TASK-3 channels may contribute to the neuromodulatory effect of spermine released from neurons during repetitive activity or during hypoxia.

MeSH Terms
Animals Calcium/administration & dosage Cations/administration & dosage Cells, Cultured Dose-Response Relationship, Drug Ion Channel Gating/drug effects,physiology Magnesium/administration & dosage Membrane Potentials/drug effects,physiology Nerve Tissue Proteins Neurons/drug effects,physiology Potassium Channels, Tandem Pore Domain/metabolism Rats Rats, Long-Evans Spermine/administration & dosage Thalamus/drug effects,physiology
Chemicals
Cations Kcnk9 protein, rat Nerve Tissue Proteins Potassium Channels, Tandem Pore Domain potassium channel subfamily K member 3 Spermine Magnesium Calcium
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Musset Boris
Institut für Physiologie, Universität Marburg, Deutschhausstrasse 2, 35037 Marburg, Germany.
Meuth Sven G
Liu Gong Xin
Derst Christian
Wegner Sven
Pape Hans-Christian
Budde Thomas
Preisig-Müller Regina
Daut Jürgen
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Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
DOI
10.1113/jphysiol.2006.106898
Published
2006-05-01
Pages
639-57
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1780017
Subset
IM
External Links
PubMed source DOI: 10.1113/jphysiol.2006.106898 PMC Full Text View journal details
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