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Translocation of diacylglycerol kinase theta from cytosol to plasma membrane in response to activation of G protein-coupled receptors and protein kinase C

Translocation of diacylglycerol kinase theta from cytosol to plasma membrane in response to activation of G protein-coupled receptors and protein kinase C
Translocation of diacylglycerol kinase theta from cytosol to plasma membrane in response to activation of G protein-coupled receptors and protein kinase C
Diacylglycerol kinase (DGK) phosphorylates the second messenger diacylglycerol (DAG) to phosphatidic acid. We previously identified DGK as one of nine mammalian DGK isoforms and reported on its regulation by interaction with RhoA and by translocation to the plasma membrane in response to noradrenaline. Here, we have investigated how the localization of DGK, fused to green fluorescent protein, is controlled upon activation of G protein-coupled receptors in A431 cells. Extracellular ATP, bradykinin, or thrombin induced DGK translocation from the cytoplasm to the plasma membrane within 2-6 min. This translocation, independent of DGK activity, was preceded by protein kinase C (PKC) translocation and was blocked by PKC inhibitors. Conversely, activation of PKC by 12-O-tetradecanoylphorbol-13-acetate induced DGK translocation. Membrane-permeable DAG (dioctanoylglycerol) also induced DGK translocation but in a PKC (staurosporin)-independent fashion. Mutations in the cysteine-rich domains of DGK abrogated its hormone- and DAG-induced translocation, suggesting that these domains are essential for DAG binding and DGK recruitment to the membrane. We show that DGK interacts selectively with and is phosphorylated by PKCepsilon and -eta and that peptide agonist-induced selective activation of PKCepsilon directly leads to DGK translocation. Our data are consistent with the concept that hormone-induced PKC activation regulates the intracellular localization of DGK, which may be important in the negative regulation of PKCepsilon and/or PKCeta activity.
Adenosine Triphosphate/metabolism Animals Blotting, Western Bradykinin/metabolism COS Cells Cell Line, Tumor Cell Membrane/*metabolism Cytoplasm/metabolism Cytosol/*metabolism DNA, Complementary/metabolism Diacylglycerol Kinase/*metabolism GTP-Binding Proteins/*metabolism Glutathione Transferase/metabolism Glycerol/chemistry Green Fluorescent Proteins/metabolism Humans Kinetics Microscopy, Confocal Models, Biological Mutation Norepinephrine/metabolism Peptides/chemistry Phosphorylation Point Mutation Protein Binding Protein Isoforms Protein Kinase C/*metabolism Protein Structure, Tertiary Protein Transport RNA, Messenger/metabolism Recombinant Fusion Proteins/metabolism Reverse Transcriptase Polymerase Chain Reaction Staurosporine/pharmacology Subcellular Fractions Tetradecanoylphorbol Acetate/chemistry Thrombin/metabolism Time Factors Transcriptional Activation
0021-9258
9870-9878
van Baal, J.
b6b47118-7a83-41f0-9bf0-c1760380ada7
de Widt, J.
8e144c94-ffc7-47c5-afe9-1dc463c3621f
Divecha, N.
5c2ad0f8-4ce7-405f-8a15-2fc4ab96d787
van Blitterswijk, W. J.
aa501394-3d66-4738-9483-b025ce31b3c7
van Baal, J.
b6b47118-7a83-41f0-9bf0-c1760380ada7
de Widt, J.
8e144c94-ffc7-47c5-afe9-1dc463c3621f
Divecha, N.
5c2ad0f8-4ce7-405f-8a15-2fc4ab96d787
van Blitterswijk, W. J.
aa501394-3d66-4738-9483-b025ce31b3c7

van Baal, J., de Widt, J., Divecha, N. and van Blitterswijk, W. J. (2005) Translocation of diacylglycerol kinase theta from cytosol to plasma membrane in response to activation of G protein-coupled receptors and protein kinase C. The Journal of Biological Chemistry, 280 (11), 9870-9878. (doi:10.1074/jbc.M409301200).

Record type: Article

Abstract

Diacylglycerol kinase (DGK) phosphorylates the second messenger diacylglycerol (DAG) to phosphatidic acid. We previously identified DGK as one of nine mammalian DGK isoforms and reported on its regulation by interaction with RhoA and by translocation to the plasma membrane in response to noradrenaline. Here, we have investigated how the localization of DGK, fused to green fluorescent protein, is controlled upon activation of G protein-coupled receptors in A431 cells. Extracellular ATP, bradykinin, or thrombin induced DGK translocation from the cytoplasm to the plasma membrane within 2-6 min. This translocation, independent of DGK activity, was preceded by protein kinase C (PKC) translocation and was blocked by PKC inhibitors. Conversely, activation of PKC by 12-O-tetradecanoylphorbol-13-acetate induced DGK translocation. Membrane-permeable DAG (dioctanoylglycerol) also induced DGK translocation but in a PKC (staurosporin)-independent fashion. Mutations in the cysteine-rich domains of DGK abrogated its hormone- and DAG-induced translocation, suggesting that these domains are essential for DAG binding and DGK recruitment to the membrane. We show that DGK interacts selectively with and is phosphorylated by PKCepsilon and -eta and that peptide agonist-induced selective activation of PKCepsilon directly leads to DGK translocation. Our data are consistent with the concept that hormone-induced PKC activation regulates the intracellular localization of DGK, which may be important in the negative regulation of PKCepsilon and/or PKCeta activity.

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More information

Published date: 18 March 2005
Additional Information: van Baal, Jurgen de Widt, John Divecha, Nullin van Blitterswijk, Wim J eng Research Support, Non-U.S. Gov't 2005/01/06 J Biol Chem. 2005 Mar 18;280(11):9870-8. doi: 10.1074/jbc.M409301200. Epub 2005 Jan 4.
Keywords: Adenosine Triphosphate/metabolism Animals Blotting, Western Bradykinin/metabolism COS Cells Cell Line, Tumor Cell Membrane/*metabolism Cytoplasm/metabolism Cytosol/*metabolism DNA, Complementary/metabolism Diacylglycerol Kinase/*metabolism GTP-Binding Proteins/*metabolism Glutathione Transferase/metabolism Glycerol/chemistry Green Fluorescent Proteins/metabolism Humans Kinetics Microscopy, Confocal Models, Biological Mutation Norepinephrine/metabolism Peptides/chemistry Phosphorylation Point Mutation Protein Binding Protein Isoforms Protein Kinase C/*metabolism Protein Structure, Tertiary Protein Transport RNA, Messenger/metabolism Recombinant Fusion Proteins/metabolism Reverse Transcriptase Polymerase Chain Reaction Staurosporine/pharmacology Subcellular Fractions Tetradecanoylphorbol Acetate/chemistry Thrombin/metabolism Time Factors Transcriptional Activation

Identifiers

Local EPrints ID: 479770
URI: http://eprints.soton.ac.uk/id/eprint/479770
ISSN: 0021-9258
PURE UUID: 7f022a6a-48bf-4a4e-aaf1-febbc6eae511

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Date deposited: 26 Jul 2023 17:00
Last modified: 17 Mar 2024 03:00

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Contributors

Author: J. van Baal
Author: J. de Widt
Author: N. Divecha
Author: W. J. van Blitterswijk

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