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J. Biol. Chem., Vol. 276, Issue 7, 4709-4716, February 16, 2001
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From the The purpose of the current study is
to investigate the effect of opioid-independent, heterologous
activation of protein kinase C (PKC) on the responsiveness of opioid
receptor and the underlying molecular mechanisms. Our result showed
that removing the C terminus of
Heterologous Activation of Protein Kinase C Stimulates
Phosphorylation of
-Opioid Receptor at Serine 344, Resulting in
-Arrestin- and Clathrin-mediated Receptor Internalization*
,,,,¶
National Laboratory of Medical Neurobiology,
Fudan University Medical Center, Shanghai 200032, and
§ Shanghai Institute of Biochemistry and Cell Biology,
Shanghai Institutes of Biological Sciences, Chinese Academy of
Sciences, Shanghai 200031, People's Republic of China
opioid receptor (DOR) containing
six Ser/Thr residues abolished both DPDPE- and phorbol 12-myristate
13-acetate (PMA)-induced DOR phosphorylation. The phosphorylation
levels of DOR mutants T352A, T353A, and T358A/T361A/S363S were
comparable to that of the wild-type DOR, whereas S344G substitution
blocked PMA-induced receptor phosphorylation, indicating that
PKC-mediated phosphorylation occurs at Ser-344. PKC-mediated
Ser-344 phosphorylation was also induced by activation of
Gq-coupled 
1A-adrenergic receptor or increase in intracellular Ca2+ concentration. Activation of
PKC by PMA, 1A-adrenergic receptor agonist, and
ionomycin resulted in DOR internalization that required phosphorylation
of Ser-344. Expression of dominant negative 
-arrestin and hypertonic
sucrose treatment blocked PMA-induced DOR internalization, suggesting
that PKC mediates DOR internalization via a -arrestin- and
clathrin-dependent mechanism. Further study demonstrated
that agonist-dependent G protein-coupled receptor kinase
(GRK) phosphorylation sites in DOR are not targets of PKC.
Agonist-dependent, GRK-mediated receptor phosphorylation
and agonist-independent, PKC-mediated DOR phosphorylation were
additive, but agonist-induced receptor phosphorylation could inhibit
PKC-catalyzed heterologous DOR phosphorylation and subsequent
internalization. These data demonstrate that the responsiveness of
opioid receptor is regulated by both PKC and GRK through
agonist-dependent and agonist-independent mechanisms and
PKC-mediated receptor phosphorylation is an important molecular mechanism of heterologous regulation of opioid receptor functions.
*
This work was supported by grants from the National Natural
Science Foundation of China (39825110 and 39625015) and the Ministry of
Science and Technology (G1999054003 and G1999053907) and by the
Ministry of Education and the Shanghai Municipal Commission of Science
and Technology.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.
Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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