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J. Biol. Chem., Vol. 276, Issue 20, 16720-16730, May 18, 2001
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From the Department of Pharmacology, University of
Virginia, Charlottesville, Virginia 22908-0735
G protein-coupled inwardly rectifying
K+ (GIRK) channels can be activated or inhibited by
distinct classes of receptor (G
Receptor-mediated Inhibition of G Protein-coupled Inwardly
Rectifying Potassium Channels Involves G
q Family
Subunits, Phospholipase C, and a Readily Diffusible Messenger*
i/o- and
Gq-coupled), providing dynamic regulation of cellular
excitability. Receptor-mediated activation involves direct effects of
G
subunits on GIRK channels, but mechanisms involved in GIRK
channel inhibition have not been fully elucidated. An HEK293 cell line
that stably expresses GIRK1/4 channels was used to test G
protein mechanisms that mediate GIRK channel inhibition. In cells
transiently or stably cotransfected with 5-HT1A
(Gi/o-coupled) and TRH-R1
(Gq-coupled) receptors, 5-HT (5-hydroxytryptamine;
serotonin) enhanced GIRK channel currents, whereas
thyrotropin-releasing hormone (TRH) inhibited both basal and
5-HT-activated GIRK channel currents. Inhibition of GIRK channel
currents by TRH primarily involved signaling by Gq
family subunits, rather than G dimers: GIRK channel current
inhibition was diminished by Pasteurella multocida toxin,
mimicked by constitutively active members of the Gq
family, and reduced by minigene constructs that disrupt
Gq signaling, but was completely preserved in cells
expressing constructs that interfere with signaling by G
subunits. Inhibition of GIRK channel currents by TRH and constitutively
active Gq was reduced by U73122, an inhibitor of
phospholipase C (PLC). Moreover, TRH- R1-mediated GIRK channel
inhibition was diminished by minigene constructs that reduce membrane
levels of the PLC substrate phosphatidylinositol bisphosphate, further
implicating PLC. However, we found no evidence for involvement of
protein kinase C, inositol trisphosphate, or intracellular calcium.
Although these downstream signaling intermediaries did not contribute
to receptor-mediated GIRK channel inhibition, bath application of TRH
decreased GIRK channel activity in cell-attached patches. Together,
these data indicate that receptor-mediated inhibition of GIRK channels
involves PLC activation by G subunits of the Gq
family and suggest that inhibition may be communicated at a distance to
GIRK channels via unbinding and diffusion of phosphatidylinositol
bisphosphate away from the channel.
*
This work was supported by National Research Service Award
Predoctoral Fellowship MH12091 (to E. M. T.) and National Institutes of Health Grant NS39553 (to D. A. B.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
To whom correspondence should be addressed: Dept. of Pharmacology,
University of Virginia Health System, P. O. Box 800735, 1300 Jefferson
Park Ave., Charlottesville, VA 22908-0735. Tel.: 804-982-4449; Fax:
804-982-3878; E-mail: dab3y@virginia.edu.
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