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J Biol Chem, Vol. 275, Issue 2, 1357-1364, January 14, 2000
From the The contribution of voltage-dependent
ion channels to nerve function depends upon their cell-surface
distributions. Nevertheless, the mechanisms underlying channel
localization are poorly understood. Two phenomena appear particularly
important: the clustering of channels by membrane-associated guanylate
kinases (MAGUKs), such as PSD-95, and the regional stabilization of
cell-surface proteins by differential suppression of endocytosis. Could
these phenomena be related? To test this possibility we examined the
effect of PSD-95 on the internalization rate of Kv1.4
K+ channels in transfected HEK293 cells using
cell-surface biotinylation assays. When expressed alone Kv1.4 was
internalized with a half-life of 87 min, but, in the presence of
PSD-95, Kv1.4 internalization was completely suppressed.
Immunochemistry and electrophysiology showed PSD-95 had little effect
on total or cell-surface levels of Kv1.4 or on current amplitude,
activation, or inactivation kinetics. Clustering was necessary and
sufficient to suppress Kv1.4 internalization since C35S-PSD-95, a
mutant reported to bind but not cluster Kv1.4, (confirmed by imaging
cells co-expressing a functional, GFP-variant-tagged Kv1.4) restored
and, surprisingly, enhanced the rate of Kv1.4 internalization
(t1/2 = 16 min). These data argue PSD-95-mediated
clustering suppresses Kv1.4 internalization and suggest a fundamentally
new role for PSD-95, and perhaps other MAGUKs, orchestrating the
stabilization of channels at the cell-surface.
Internalization of the Kv1.4 Potassium Channel Is Suppressed by
Clustering Interactions with PSD-95*
§,¶,¶, and§
Division of Cellular and Molecular Biology,
Toronto Western Research Institute, University Health Network, Toronto,
Ontario M5T 2S8, Canada, the § Department of Pharmacology,
University of Toronto, Toronto, Ontario M5S 1A8, Canada, and the
¶ Department of Physiology, University of Toronto, Toronto,
Ontario M5S 1A8, Canada
*
This work was supported by awards from the Natural Sciences
and Engineering Research Council of Canada (to O. T. J), the
Medical Research Council of Canada (to L. C. S), a studentship
from the Bloorview Epilepsy Program (to D. G. M. J.),
and a Santalo scholarship from the University of Toronto (to R. K).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: Div. of Cellular
and Molecular Biology, Toronto Western Research Institute, University Health Network, MC 11-434, 399 Bathurst St., Toronto, Ontario M5T 2S8,
Canada. Tel.: 416-603-5039; Fax: 416-603-5745; E-mail: owen@playfair.utoronto.ca.
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