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Vol. 53, Issue 6, 1047-1053, June 1998
3 Phosphorylation to the Rapid
Attenuation of Opioid-Activated Phosphoinositide Response
Department of Pharmacology, University of Minnesota, Minneapolis,
Minnesota 55455-0347
Activation of the 
-opioid receptor in NG108-15 neuroblastoma X
glioma hybrid cells results in a transient increase at the intracellular level of inositol-1,4,5-triphosphate
[Ins(1,4,5)P3]. This time course in the transient increase in the
Ins(1,4,5)P3 level is distinctly different from that observed in the
homologous opioid receptor desensitization as measured by the
inhibition of adenylyl cyclase activity. One probable mechanism for
this rapid loss in Ins(1,4,5)P3 response is the feedback regulation of
the phospholipase C activity. Regulation by protein phosphorylation was
suggested by the observations that the opioid-mediated response was
potentiated by calphostin C, an inhibitor of protein kinase C (PKC),
and was abolished by either phorbol-12-myristate-13-acetate, a
PKC activator, or calyculin A, a protein
phosphatase1/2A inhibitor. The direct
phosphorylation of phospholipase C was demonstrated by
immunoprecipitation of PLC-
3 from metabolically labeled NG108-15 cells challenged with the -selective agonist
[D-Pen2,D-Pen5]enkephalin
(DPDPE). A time- and DPDPE concentration-dependent and
naloxone-reversible increase in the PLC-3 phosphorylation can be
demonstrated. This PLC-3 phosphorylation was mainly due to PKC
activation because pretreatment of NG108-15 cells with calphostin C
could block the DPDPE effect. Activation of the PLC-3 by DPDPE was
one of the prerequisites for agonist-mediated PLC-3 phosphorylation
because the aminosteroid phospholipase C inhibitor U73122 could block
the DPDPE effect. In addition to DPDPE, lysophosphatidic acid (LPA)
stimulated the PLC-3 phosphorylation, but bradykinin did not.
Furthermore, the LPA- and DPDPE-mediated PLC-3 phosphorylation was
additive and was much less than that observed with
phorbol-12-myristate-13-acetate. The effect of DPDPE was specific to
PLC-3; the 
-insensitive phospholipase C-1 was not
phosphorylated in the presence of either DPDPE or LPA. These results
indicate that although PKC phosphorylation of PLC-3 is not
obligatory for the opioid receptor desensitization, it seems to play a
significant facilatory role in the mechanisms allowing desensitization
of opioid-activated phospholipase C response before that of adenylyl
cyclase inhibition.
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