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Vol. 60, Issue 6, 1243-1253, December 2001
-Arrestin1 Isoform-Specific
The John. P. Robarts Research Institute (L.B.D., M.B.,
J.L.S., P.H.A., S.S.G.F.) and Departments of Pharmacology and
Toxicology (S.S.G.), Physiology (J.L.S., S.S.G.), and
Medicine (S.S.G.), University of Western Ontario, London, Ontario,
Canada
Metabotropic glutamate receptors (mGluRs) are G protein-coupled
receptors (GPCRs) that contribute to the regulation of integrative brain functions such as cognition, motor control, and neural
development. Metabotropic glutamate receptors are members of a unique
class of GPCRs (class III) that include the calcium sensing and
-aminobutyric acid type B receptors. Although mGluRs bear little
sequence homology to well-characterized members of the GPCR
superfamily, both second messenger-dependent protein kinases and G
protein-coupled receptor kinases (GRKs) contribute to mGluR
desensitization. Therefore, in the present study, we examined whether
-arrestins, regulators of GPCR desensitization and endocytosis, are
required for mGluR1a desensitization and internalization in human
embryonic kidney (HEK) 293 cells. Unlike what has been reported for
other GPCRs, we find that in response to agonist stimulation, mGluR1a
internalization is selectively mediated by -arrestin1 in HEK 293 cells. However, even though -arrestin1 binds directly to the
carboxyl-terminal tail of mGluR1a and redistributes with mGluR1a to
endosomes, neither -arrestin1 nor -arrestin2 seems to contribute
to mGluR1a desensitization in HEK 293 cells. We also observed extensive
tonic mGluR1a internalization via clathrin-coated vesicles in the
absence of agonist. The tonic internalization of mGluR1a is insensitive
to antagonist treatment, dominant-negative mutants of GRK2,
-arrestin1, and dynamin as well as treatments that disrupt caveolae,
but is blocked by hypertonic sucrose and concanavalin A treatment.
Internalized mGluR1a is colocalized with clathrin, transferrin
receptor, 2-adrenergic receptor, and Rab5 GTPase in
endocytic vesicles. Therefore, although mGluR1a internalizes with
-arrestin in response to agonist, the agonist-independent
internalization of mGluR1a involves the -arrestin-independent targeting of mGluR1a to clathrin-coated vesicles.
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