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Originally published In Press as doi:10.1074/jbc.M211053200 on November 25, 2002

J. Biol. Chem., Vol. 278, Issue 7, 5419-5426, February 14, 2003
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Protein Kinase C Isoform-specific Differences in the Spatial-Temporal Regulation and Decoding of Metabotropic Glutamate Receptor1a-stimulated Second Messenger Responses*

Andy V. BabwahDagger §, Lianne B. DaleDagger §, and Stephen S. G. FergusonDagger ||**Dagger Dagger

From the Dagger  Cell Biology Research Group, Robarts Research Institute, and the || Department of Physiology & Pharmacology, University of Western Ontario, 100 Perth Drive, London, Ontario N6A 5K8, Canada

Metabotropic glutamate receptors (mGluRs) coupled via Gq to the hydrolysis of phosphoinositides stimulate Ca2+ and PKCbeta II oscillations in both excitable and non-excitable cells. In the present study, we show that mGluR1a activation stimulates the repetitive plasma membrane translocation of each of the conventional and novel, but not atypical, PKC isozymes. However, despite similarities in sequence and cofactor regulation by diacyglycerol and Ca2+, conventional PKCs exhibit isoform-specific oscillation patterns. PKCalpha and PKCbeta I display three distinct patterns of activity: 1) agonist-independent oscillations, 2) agonist-stimulated oscillations, and 3) persistent plasma membrane localization in response to mGluR1a activation. In contrast, only agonist-stimulated PKCbeta II translocation responses are observed in mGluR1a-expressing cells. PKCbeta I expression also promotes persistent increases in intracellular diacyglycerol concentrations in response to mGluR1a stimulation without affecting PKCbeta II oscillation patterns in the same cell. PKCbeta II isoform-specific translocation patterns are regulated by specific amino acid residues localized within the C-terminal PKC V5 domain. Specifically, Asn-625 and Lys-668 localized within the V5 domain of PKCbeta II cooperatively suppress PKCbeta I-like response patterns for PKCbeta II. Thus, redundancy in PKC isoform expression and differential decoding of second messenger response provides a novel mechanism for generating cell type-specific responses to the same signal.

* This work was supported by Canadian Institutes of Health Research Grant MA-15506 (to S. S. G. F.).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.

§ These authors contributed equally to this work.

Recipient of a Canadian Hypertension Society/CIHR fellowship.

** Recipient of Heart and Stroke Foundation of Canada MacDonald Scholarship, Premier's Research Excellence Award, and Canada Research Chair in Molecular Neuroscience.

Dagger Dagger To whom correspondence should be addressed: Robarts Research Inst., 100 Perth Dr., P.O. Box 5015, London, Ontario N6A 5K8, Canada. Tel.: 519-663-3825; Fax: 519-663-3789; E-mail: ferguson@robarts.ca.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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