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Originally published In Press as doi:10.1074/jbc.M009144200 on February 14, 2001

J. Biol. Chem., Vol. 276, Issue 18, 14980-14986, May 4, 2001
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Protein Kinase C alpha -mediated Negative Feedback Regulation Is Responsible for the Termination of Insulin-like Growth Factor I-induced Activation of Nuclear Phospholipase C beta 1 in Swiss 3T3 Cells*

Aimin XuDagger , Yu Wang§, Lance Yi XuDagger , and R. Stewart GilmourDagger

From the Dagger  Liggins Institute, School of Medicine, and § School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand

Previous studies from several independent laboratories have demonstrated the existence of an autonomous phosphoinositide (PI) cycle within the nucleus, where it is involved in both cell proliferation and differentiation. Stimulation of Swiss 3T3 cells with insulin-like growth factor-I (IGF-I) has been shown to induce a transient and rapid increase in the activity of nuclear-localized phospholipase C (PLC) beta 1, which in turn leads to the production of inositol trisphosphate and diacylglycerol in the nucleus. Nuclear diacylglycerol provides the driving force for the nuclear translocation of protein kinase C (PKC) alpha . Here, we report that treatment of Swiss 3T3 cells with Go6976, a selective inhibitor of PKC alpha , caused a sustained elevation of IGF-I-stimulated nuclear PLC activity. A time course study revealed an inverse relationship between nuclear PKC activity and the activity of nuclear PLC in IGF-I-treated cells. A time-dependent association between PKC alpha  and PLC beta 1 in the nucleus was also observed following IGF-I treatment. Two-dimensional phosphopeptide mapping and site-directed mutagenesis demonstrated that PKC promoted phosphorylation of PLC beta 1 at serine 887 in the nucleus of IGF-I-treated cells. Overexpression of either a PLC beta 1 mutant in which the PKC phosphorylation site Ser887 was replaced by alanine, or a dominant-negative PKC alpha , resulted in a sustained activation of nuclear PLC following IGF-I stimulation. These results indicate that a negative feedback regulation of PLC beta 1 by PKC alpha  plays a critical role in the termination of the IGF-I-dependent signal that activates the nuclear PI cycle.

* This work was supported by the Marsden Fund of the Royal Society of New Zealand and Health Research Council of New Zealand.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. Fax: 64-9-3737492; E-mail: s.gilmour@auckland.ac.nz.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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