Heteromeric TASK-1/TASK-3 is the major oxygen-sensitive background K+ channel in rat carotid body glomus cells.

Full Abstract

Carotid body (CB) glomus cells from rat express a TASK-like background K+ channel that is believed to play a critical role in the regulation of excitability and hypoxia-induced increase in respiration. Here we studied the kinetic behaviour of single channel openings from rat CB cells to determine the molecular identity of the 'TASK-like' K+ channels. In outside-out patches, the TASK-like background K+ channel in CB cells was inhibited >90% by a reduction of pH(o) from 7.3 to 5.8. In cell-attached patches with 140 mM KCl and 1 mM Mg2+ in the bath and pipette solutions, two main open levels with conductance levels of approximately 14 pS and approximately 32 pS were recorded at a membrane potential of -60 mV. The K+ channels showed kinetic properties similar to TASK-1 (approximately 14 pS), TASK-3 (approximately 32 pS) and TASK-1/3 heteromer (approximately 32 pS). The presence of three TASK isoforms was tested by reducing [Mg2+](o) to approximately 0 mM, which had no effect on the conductance of TASK-1, but increased those of TASK-1/3 and TASK-3 to 42 pS and 74 pS, respectively. In CB cells, the reduction of [Mg2+](o) to approximately 0 mM also caused the appearance of approximately 42 pS (TASK-1/3-like) and approximately 74 pS (TASK-3-like) channels, in addition to the approximately 14 pS (TASK-1-like) channel. The 42 pS channel was the most abundant, contributing approximately 75% of the current produced by TASK-like channels. Ruthenium red (5 microM) had no effect on TASK-1 and TASK-1/3, but inhibited TASK-3 by 87%. In CB cells, ruthenium red caused approximately 12% inhibition of TASK-like activity. Methanandamide reduced the activity of all three TASKs by 80-90%, and that of TASK-like channels in CB cell also by approximately 80%. In CB cells, hypoxia caused inhibition of TASK-like channels, including TASK-1/3-like channels. These results show that TASK-1, TASK-1/3 and TASK-3 are all functionally expressed in isolated CB cells, and that the TASK-1/3 heteromer provides the major part of the oxygen-sensitive TASK-like background K+ conductance.

Author information

Author/s: Kim, Donghee (D); Cavanaugh, Eric J (EJ); Kim, Insook (I); Carroll, John L (JL);

Affiliation: Department of Physiology and Biophysics, Rosalind Franklin University of Medicine and Science, The Chicago Medical School, 3333 Green Bay Road, North Chicago, IL 60064, USA.

Grants: HL054621 (Agency:NHLBI NIH HHS) ; R01 HL054621-10 (Agency:NHLBI NIH HHS)

Journal and publication information

Publication Type: Journal Article; Research Support, N.I.H., Extramural

Journal: The Journal of physiology (J Physiol), published in England. (Language: eng)

Reference: 2009-Jun; vol 587 (issue Pt 12) : pp 2963-75

Dates: Created 2009/06/15; Completed 2009/09/21; Revised 2009/11/16;

PMID: 19403596, status: MEDLINE (last retrieved date: 11/17/2009)

Sourced from the National Library of Medicine. Abstract text and other information may be subject to copyright.

Comments and Corrections

CommentIn: J Physiol. 2009 Jun 15;587(Pt 12):2717-8. (PMID: 19525556)

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MeSH headings (categories)

This article was linked to the MeSH Headings (categories) shown below.

Animals
Arachidonic Acids - pharmacology
Carotid Body - cytology; drug effects; physiology
Cell Hypoxia - physiology
Coloring Agents
Electrophysiology
Hela Cells
Humans
Isomerism
Magnesium - pharmacology

Magnesium - pharmacology
Membrane Potentials - drug effects
Nerve Tissue Proteins - drug effects; metabolism
Oxygen - physiology
Patch-Clamp Techniques
Potassium Channel Blockers - pharmacology
Potassium Channels, Tandem Pore Domain - drug effects; metabolism
RNA, Messenger - biosynthesis; genetics
Rats
Ruthenium Red

Note: Bold headings indicate primary MeSH headings or qualifiers.

Associated Chemicals: Arachidonic Acids (0) ; Coloring Agents (0) ; KCNK9 protein, human (0) ; Nerve Tissue Proteins (0) ; Potassium Channel Blockers (0) ; Potassium Channels, Tandem Pore Domain (0) ; RNA, Messenger (0) ; potassium channel subfamily K member 3 (0) ; Ruthenium Red (11103-72-3) ; methanandamide (150314-39-9) ; Magnesium (7439-95-4) ; Oxygen (7782-44-7)

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