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J. Biol. Chem., Vol. 279, Issue 28, 29501-29512, July 9, 2004
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*
From the Department of Chemistry, University of Illinois, Chicago, Illinois 60607
The regulatory domains of novel protein kinases C (PKC) contain two C1 domains (C1A and C1B), which have been identified as the interaction site for sn-1,2-diacylglycerol (DAG) and phorbol ester, and a C2 domain that may be involved in interaction with lipids and/or proteins. Although recent reports have indicated that C1A and C1B domains of conventional PKCs play different roles in their DAG-mediated membrane binding and activation, the individual roles of C1A and C1B domains in the DAG-mediated activation of novel PKCs have not been fully understood. In this study, we determined the roles of C1A and C1B domains of PKC
by means of in vitro lipid binding analyses and cellular protein translocation measurements. Isothermal titration calorimetry and surface plasmon resonance measurements showed that isolated C1A and C1B domains of PKC have opposite affinities for DAG and phorbol ester; i.e. the C1A domain with high affinity for DAG and the C1B domain with high affinity for phorbol ester. Furthermore, in vitro activity and membrane binding analyses of PKC mutants showed that the C1A domain is critical for the DAG-induced membrane binding and activation of PKC. The studies also indicated that an anionic residue, Glu177, in the C1A domain plays a key role in controlling the DAG accessibility of the conformationally restricted C1A domain in a phosphatidylserine-dependent manner. Cell studies with enhanced green fluorescent protein-tagged PKC and mutants showed that because of its phosphatidylserine specificity PKC preferentially translocated to the plasma membrane under the conditions in which DAG is randomly distributed among intracellular membranes of HEK293 cells. Collectively, these results provide new insight into the differential roles of C1 domains in the DAG-induced membrane activation of PKC and the origin of its specific subcellular localization in response to DAG.
Received for publication, March 22, 2004 , and in revised form, April 16, 2004.
* This work was supported by National Institutes of Health Grants GM52598, GM53987, and GM68849. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Present address: Dept. of Cell Biology, Yale University School of Medicine, P. O. Box 208002, 333 Cedar St., New Haven, CT 06520-8002.
To whom correspondence should be addressed: M/C 111, 845 West Taylor St., Chicago, IL 60607-7061. Tel.: 312-996-4883; Fax: 312-996-2183; E-mail: wcho{at}uic.edu.
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