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Diabetes Publish Ahead of Print published online ahead of print June 6, 2002
DOI: 10.2337/diabetes.51.7.2018
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Received for publication 14 March 2002
Accepted in revised form 10 May 2002

Critical Role for Cataplerosis via Citrate in Glucose-Regulated Insulin Release

Daisy Flamez 1 , Veerle Berger 1 , Mogens Kruhøffer 2 , Torben Orntoft 2 , Daniel Pipeleers 3 , and Frans C. Schuit 1 *

From the 1 Molecular Pharmacology Unit, Diabetes Research Center, Faculty of Medicine, Vrije Universiteit Brussel, Brussels, Belgium, 2 Molecular Diagnostic Laboratory, Aarhus University Hospital, Aarhus, Denmark, and 3 Cell Therapy Unit, Diabetes Research Center, Faculty of Medicine, Vrije Universiteit Brussel, Brussels, Belgium

* Address correspondence and reprint requests to Frans C. Schuit. Email: fschuit{at}minf.vub.ac.be.

The molecular mechanisms mediating acute regulation of insulin release by glucose are partially known. The process involves at least two pathways that can be discriminated on basis of their (in)dependence of closure of ATP-sensitive potassium (K+ATP) channels. The mechanism of the K+ATP channel--independent pathway was proposed to involve cataplerosis, the export of mitochondrial intermediates into the cytosol and in the induction of fatty acid--derived signaling molecules. In the present article, we have explored in fluorescence-activated cell sorter (FACS)-purified rat ß-cells the molecular steps involved in chronic glucose regulation of the insulin secretory response. When compared with culture in 10 mmol/l glucose, 24 h culture in 3 mmol/l glucose shifts the phenotype of the cells into a state with low further secretory responsiveness to glucose, lower rates of glucose oxidation, and lower rates of cataplerosis. Microarray mRNA analysis indicates that this shift can be attributed to differences in expression of genes involved in the K+ATP channel--dependent pathway, in cataplerosis and in fatty acid/cholesterol biosynthesis. This response was paralleled by glucose upregulation of the transcription factor sterol regulatory element binding protein 1c (SREBP1c) (ADD1) and downregulation of peroxisome proliferator—activated receptor (PPAR)-{alpha} and PPAR-ß (PPAR{delta}). The functional importance of cataplerosis via citrate for glucose-induced insulin release was further supported by the observation that two ATP-citrate lyase inhibitors, radicicol and (-)-hydroxycitrate, block part of glucose-stimulated release in ß-cells. In conclusion, chronic glucose regulation of the glucose-responsive secretory phenotype is associated with coordinated changes in gene expression involved in the K+ATP channel--dependent pathway, in cataplerosis via citrate and in acyl CoA/cholesterol biosynthesis.


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