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J Biol Chem, Vol. 274, Issue 16, 10999-11006, April 16, 1999
-Arrestin
Endocytic Complexes
,,,, and
From the Howard Hughes Medical Institute
Laboratories, Departments of Cell Biology and Medicine, Duke University
Medical Center, Durham, North Carolina 27710 and the § John
P. Robarts Research Institute, Departments of Physiology and
Pharmacology and Toxicology, University of Western Ontario, P.O. Box
5015, 100 Perth Drive, London, Ontario N6A 5K8, Canada
-Arrestins are multifunctional
proteins identified on the basis of their ability to bind and uncouple
G protein-coupled receptors (GPCR) from heterotrimeric G proteins. In
addition, -arrestins play a central role in mediating GPCR
endocytosis, a key regulatory step in receptor resensitization. In this
study, we visualize the intracellular trafficking of -arrestin2 in
response to activation of several distinct GPCRs including the
2-adrenergic receptor (2AR),
angiotensin II type 1A receptor (AT1AR), dopamine D1A receptor (D1AR), endothelin type A receptor
(ETAR), and neurotensin receptor (NTR). Our results reveal
that in response to 2AR activation, -arrestin2
translocation to the plasma membrane shares the same pharmacological
profile as described for receptor activation and sequestration,
consistent with a role for -arrestin as the agonist-driven switch
initiating receptor endocytosis. Whereas redistributed -arrestins
are confined to the periphery of cells and do not traffic along with
activated 2AR, D1AR, and ETAR in
endocytic vesicles, activation of AT1AR and NTR triggers a
clear time-dependent redistribution of -arrestins to
intracellular vesicular compartments where they colocalize with
internalized receptors. Activation of a chimeric AT1AR with
the 2AR carboxyl-terminal tail results in a -arrestin
membrane localization pattern similar to that observed in response to
2AR activation. In contrast, the corresponding chimeric
2AR with the AT1AR carboxyl-terminal tail
gains the ability to translocate -arrestin to intracellular
vesicles. These results demonstrate that the cellular trafficking of
-arrestin proteins is differentially regulated by the activation of
distinct GPCRs. Furthermore, they suggest that the carboxyl-tail of the receptors might be involved in determining the stability of
receptor/arrestin complexes and cellular distribution of
-arrestins.
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